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Cyanobacteria are the Earth's oldest oxygenic photoautotrophs and have had major impacts on shaping its biosphere. Their long evolutionary history (∼3.5 by) has enabled them to adapt to geochemical and climatic changes, and more recently anthropogenic modifications of aquatic environments, including nutrient over-enrichment (eutrophication), water diversions, withdrawals, and salinization. Many cyanobacterial genera exhibit optimal growth rates and bloom potentials at relatively high water temperatures; hence global warming plays a key role in their expansion and persistence. Bloom-forming cyanobacterial taxa can be harmful from environmental, organismal, and human health perspectives by outcompeting beneficial phytoplankton, depleting oxygen upon bloom senescence, and producing a variety of toxic secondary metabolites (e.g., cyanotoxins). How environmental factors impact cyanotoxin production is the subject of ongoing research, but nutrient (N, P and trace metals) supply rates, light, temperature, oxidative stressors, interactions with other biota (bacteria, viruses and animal grazers), and most likely, the combined effects of these factors are all involved. Accordingly, strategies aimed at controlling and mitigating harmful blooms have focused on manipulating these dynamic factors. The applicability and feasibility of various controls and management approaches is discussed for natural waters and drinking water supplies. Strategies based on physical, chemical, and biological manipulations of specific factors show promise; however, a key underlying approach that should be considered in almost all instances is nutrient (both N and P) input reductions; which have been shown to effectively reduce cyanobacterial biomass, and therefore limit health risks and frequencies of hypoxic events.
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ENVIRONMENTAL MICROBIOLOGY
Harmful Cyanobacterial Blooms: Causes, Consequences,
and Controls
Hans W. Paerl &Timothy G. Otten
Received: 7 September 2012 /Accepted: 9 December 2012
#Springer Science+Business Media New York 2013
Abstract Cyanobacteria are the Earths oldest oxygenic
photoautotrophs and have had major impacts on shaping
its biosphere. Their long evolutionary history (3.5 by)
has enabled them to adapt to geochemical and climatic
changes, and more recently anthropogenic modifications of
aquatic environments, including nutrient over-enrichment
(eutrophication), water diversions, withdrawals, and saliniza-
tion. Many cyanobacterial genera exhibit optimal growth rates
and bloom potentials at relatively high water temperatures;
hence global warming plays a key role in their expansion and
persistence. Bloom-forming cyanobacterial taxa can be harm-
ful from environmental, organismal, and human health per-
spectives by outcompeting beneficial phytoplankton,
depleting oxygen upon bloom senescence, and producing a
variety of toxic secondary metabolites (e.g., cyanotoxins).
How environmental factors impact cyanotoxin production is
the subject of ongoing research, but nutrient (N, P and trace
metals) supply rates, light, temperature, oxidative stressors,
interactions with other biota (bacteria, viruses and animal
grazers), and most likely, the combined effects of these factors
are all involved. Accordingly, strategies aimed at controlling
and mitigating harmful blooms have focused on manipulating
these dynamic factors. The applicability and feasibility of
various controls and management approaches is discussed
for natural waters and drinking water supplies. Strategies
based on physical, chemical, and biological manipulations
of specific factors show promise; however, a key under-
lying approach that should be considered in almost all
instances is nutrient (both N and P) input reductions;
which have been shown to effectively reduce cyanobacte-
rial biomass, and therefore limit health risks and frequen-
cies of hypoxic events.
Introduction
Cyanobacteria (blue-green algae) are the Earthsoldest
known oxygenic photoautotrophs. Their proliferation
during the Precambrian era (3.5 bya) dramatically al-
tered the previously anoxic biosphere which led to the
evolution of higher terrestrial plant and animal life
[129]. Many genera have the ability to fix atmospheric
nitrogen (N
2
) (an anaerobic process)[45], while they can
store phosphorus (P) and sequester iron (Fe) and a
range of essential trace metals [15,165,166]. These
traits have enabled them to exploit both nutrient-scarce
and nutrient-enriched, diverse terrestrial and aquatic
environments worldwide. In modern times, cyanobacte-
ria have exhibited ecophysiological strategies allowing
them to exploit anthropogenic modifications of these
environments; specifically nutrient over-enrichment and
hydrologic alterations to ecosystems with dramatic exam-
ples spanning the globe from alpine lakes to coastal oceans
[39,94,108,113,119].
The most obvious and troublesome sign of their contem-
porary ecological successis increasingly frequent and
highly visible harmful cyanobacterial blooms, or
CyanoHABs (Fig. 1)[59]. The harmfulaspect of these
blooms from an environmental context begins with a loss
of water clarity, which suppresses aquatic macrophytes, and
negatively affecting invertebrate and fish habitats. Bacterial
decomposition of dying blooms may lead to oxygen deple-
tion (hypoxia and anoxia), and subsequent fish kills. In
H. W. Paerl (*):T. G. Otten
Institute of Marine Sciences,
University of North Carolina at Chapel Hill, 3431 Arendell Street,
28557 Morehead City, NC, USA
e-mail: hpaerl@email.unc.edu
T. G. Otten
Department of Microbiology, Oregon State University,
220 Nash Hall,
97331 Corvallis, OR, USA
e-mail: ottent@onid.orst.edu
Microb Ecol
DOI 10.1007/s00248-012-0159-y
addition, many CyanoHABs produce toxic secondary
metabolites which can cause serious, acute intoxication in
mammals (including humans) affecting the hepatopancre-
atic, digestive, endocrine, dermal, and nervous systems [14,
17,19](Table1). Some of the most common toxin-
producing cyanobacteria include the N
2
-fixing genera:
Anabaena,Aphanizomenon,Cylindrospermopsis,Lyngbya,
Nodularia,Oscillatoria, and Trichodesmium; and the non-
N
2
fixers: Microcystis and Planktothrix (Fig. 2). Several of
these genera thrive in both fresh- and estuarine environ-
ments and some are also found in marine systems.
CyanoHABs threaten the ecological integrity and sustain-
ability of aquatic ecosystems depended upon for drinking
water, irrigation, fishing, and recreation. Recurring blooms
can be found in some of the worlds largest inland freshwater
ecosystems, including: Lake Victoria (Africa), Lake Erie and
Lake Michigan (USACanada), Lake Okeechobee (Florida,
USA), Lake Ponchartrain (Louisiana, USA), Lake Taihu
(China), and estuarine and coastal waters, e.g., the Baltic Sea,
Caspian Sea, tributaries of Chesapeake Bay, North Carolinas
Albemarle-Pamlico Sound, Florida Bay, the Swan River
Estuary in Australia, the Patos, and other coastal lagoonal
estuaries in Brazil, to mention a few [105].
Environmental Factors Controlling CyanoHAB
Dynamics
Nutrient Inputs
There is broad agreement that nutrient over-enrichment of
freshwater and marine ecosystems from anthropogenic sour-
ces (urban, agricultural, and industrial) has promoted
CyanoHAB expansion and persistence [59,97,105,106].
Phosphorus has traditionally been considered the principle
nutrient limiting primary productivity and algal biomass
Fig. 1 Harmful cyanobacterial
blooms (CyanoHABs) in a vari-
ety of aquatic environments.
Where known, specific genera
are indicated. adRemote sens-
ing views of surafe blooms in; a
Lake Taihu, China (Microcystis
spp.) (courtesy NASA MODIS),
bLake Erie, USACanada
(Microcystis) (courtesy NASA
MODIS, cLake Atitlan,
Guatamala (Lyngbya) (courtesy
NASA MODIS), dBaltic
Sea-Gulf of Finland (Nodularia,
Anabaena,Microcystis)(cour-
tesy NASA MODIS). eLake
Dianchi, China (Aphanizomenon
sp.) (courtesy Chinese
Academy of Sciences).
fand gLake Tahiu, China
(Microcystis spp.) (Photos by
H. Paerl). hTaivallahti Bay,
Baltic Sea, Finland (Finnish
Environment Institute-SYKE). i
Neuse River Estuary, North
Carolina, USA (Microcystis sp.)
(photo H. Paerl). jSt. Johns
River, FL (photo, J. Burns).k
Baltic Sea, Gulf of Finland
(Nodularia) (Finnish Border
Guard). lSanibel Inlet, coastal
Gulf of Mexico, Florida
USA (Trichodesmium sp.)
(photo, H. Paerl)
H. W. Paerl, T. G. Otten
accumulation in freshwater ecosystems [75,127]; whereas
N inputs are often cited as controlling newproduction in
the marine environment [4,88,101]. Estuarine systems tend
to fall between these nutrient limitation paradigms,with P
limited conditions often characterizing the low salinity oligo-
haline (<5), upstream regions, and N limitation typifying more
saline (>5), downstream waters [23,38,101]. Phosphorus
enrichment, especially relative to N enrichment, may favor
the development of CyanoHABs, especially N
2
fixing cyano-
bacterial genera which can supply their own N needs by
enzymatically converting atmospheric N (N
2
) to biologically
available ammonia (NH
3
)[28,39,45]. Nutrient-enriched
water bodies are especially prone to CyanoHABs if they also
have long residence times (low flushing rates), water temper-
atures periodically exceeding 20 °C, calm surface waters and
persistent vertical stratification [94,119,134]. While these
conditions are most common in freshwaters, some brackish
systems such as the estuaries of the Baltic Sea and oligohaline
regions of rivers (Albemarle-Pamlico Sound, Chesapeake
Bay, San Francisco Bay Delta), as well as geographically-
diverse lagoons, can support CyanoHABs, especially if they
experience periods of low flushing (long residence times) and
vertical stratification [67,94,98].
High P (relative to N) loading is not a universal trigger
for CyanoHAB formation. Agricultural, urban, and industrial
nutrient sources have accelerated rapidly in the past several
decades, with N loads frequently eclipsing P inputs [33,47,
115,157]. This change is attributable to increased application
of N-fertilizers, human and agricultural wastes, stormwater
runoff, groundwater discharge and atmospheric deposition;
all of which can be rich in N relative to P, leading to elevated
N loading in already nutrient-impacted water bodies [6,96,
115]. Nitrogen-rich aquatic ecosystems (high N:P) can also
be plagued by CyanoHABs, especially non-N
2
-fixing genera
[98]. These primarily include Microcystis and Planktothrix
species, although other non-N
2
-fixing genera such as
Aphanocapsa,Raphidiopsis, and Woronochinia, are all capa-
ble of aggressive expansion in N-enriched waters. While in
many instances, total maximum daily loads (TMDL) for P
have been established and implemented, N inputs remain
less strictly controlled, and as a result have increased in
many systems. N augmentation, in both developed and de-
veloping regions [46,157], has raised concerns that exces-
sive N loading is accelerating eutrophication and promoting
CyanoHABs in downstream freshwater and marine ecosys-
tems [33,102].
Therefore, the P onlyparadigm for control of CyanoHAB
blooms [128] needs to be revised [21,73,130]. This approach
was based on the assumption that N
2
fixation supplies all the
physiological needs for CyanoHABs, and therefore control of
N inputs was considered unneccesary [127]. Recent studies,
however, have shown that cyanobacterial N
2
fixation does not
meet phytoplankton or ecosystem N demands [36,73,104,
130] for several reasons, including: (1) N
2
fixation has high
energy requirements, (2) oxygen production by photosynthesis
in blooms can inhibit this anaerobic process, (3) turbulence and
Table 1 Major harmful cyanobacterial bloom-forming genera and their known toxins
Toxin Detection method(s) CyanoHAB genera
Aeruginosin HPLC, MS Microcystis,Planktothrix
Anatoxin-a/homoanatoxin-a ELISA, HPLC, MS Anabaena,Aphanizomenon,Cylindrospermopsis,Lyngbya,
Oscillatoria,Phormidium,Planktothrix,Raphidiopsis,Woronichinia
Anatoxin-a(S) AEIA, MS Anabaena
Aplysiatoxins MS Lyngbya,Oscillatoria,Schizothrix
beta-Methylamino-L-alanine
(BMAA)
ELISA,HPLC, MS Anabaena,Aphanizomenon,Calothrix,Cylindrospermopsis,Lyngbya,
Microcystis,Nostoc,Nodularia,Planktothrix,Phormidium,Prochlorococcus,
Scytonema,Synechococcus,Trichodesmium
Cyanopeptolin HPLC, MS Anabaena,Microcystis,Planktothrix
Cylindrospermopsin ELISA, HPLC, MS Anabaena,Aphanizomenon,Cylindrospermopsis,Oscillatoria,
Raphidiopsis,Umezakia
Jamaicamides MS Lyngbya
Lyngbyatoxin HPLC, MS Lyngbya
Microcystin ELISA, HPLC, MS, PPIA Anabaena,Anabaenopsis,Aphanizomenon,Aphanocapsa,Cylindrospermopsis,
Gloeotrichia,Hapalosiphon,Microcystis,Nostoc,Oscillatoria,
Phormidium,Planktothrix,Pseudoanabaena,Synechococcus,Woronochinia
Nodularin ELISA, HPLC, MS, PPIA Nodularia
Saxitoxin ELISA, HPLC, MS Anabaena,Aphanizomenon,Cylindrospermopsis,Lyngbya,
Oscillatoria,Planktothrix
AEIA acetylcholine esterase inhibition assay, ELISA enzyme-linked immunosorbent assay, HPLC high-performance liquid chromatography, MS
mass spectrometry, PPIA protein phosphatase inhibition assay
Harmful Cyanobacterial Blooms: Causes, Consequences, and Controls
wind mixing can disrupt N
2
fixation, and (4) other
cofactors may be limiting such as Fe, Mo, and/or other trace
metals [57,84,95].
In water bodies where N
2
fixation fails to meet ecosystem-
level N requirements, external N inputs play a crucial role in
enhancing fertility, with excessive N inputs often leading to
undesirable excessive algal production. Hence, eutrophic sys-
tems already subject to CyanoHAB events are prone to further
expansion of these blooms due to additional N inputs, espe-
cially if they already contain sufficient autochthonous P.
Indeed, eutrophic systems worldwide exhibit the capacity to
absorb increasing amounts of N as they increase their trophic
states [4,33,101]. Recent surveys of algal productivity in
response to nutrient enrichment across geographically diverse
eutrophic lakes, reservoirs, estuarine and coastal waters and a
range of experimental enclosures (<1 L to over 10,000 L)
reveal that strongest stimulation is routinely observed in re-
sponse to both N and P additions; indicating nutrient co-
limitation is widespread [35,74,100,107,139,140]. These
results strongly suggest that reductions in both N and P
inputs are needed to stem eutrophication and CyanoHAB
expansion [74,106,172].
Climate Change and CyanoHAB Expansion
While nutrient over-enrichment promotes CyanoHABs [59,
98], climate change provides an additional catalyst for their
expansion. Rising global temperatures and changing precipi-
tation patterns both stimulate CyanoHABs [64,99,103,106,
110]. Warmer temperatures favor surface bloom-forming cya-
nobacterial genera because they are adapted to hot conditions
and their maximal growth rates occur at relatively high tem-
peratures; often in excess of 25 °C [12,40,120,122]. At these
elevated temperatures, cyanobacteria routinely outcompete
eukaryotic algae [32,64,105,164]. Specifically, as the growth
rates of the eukaryotic taxa decline in response to warming,
cyanobacterial growth rates reach their optima (Fig. 3). Warm
surface waters are also prone to intense vertical stratification.
The strength of vertical stratification depends on the density
difference between the warm surface layer and the cold water
beneath. In marine systems, salinity gradients also induce
stratification. As temperatures rise due to climate change,
waters will begin to stratify earlier in the spring and the
stratification will persist longer into the fall [111,142,143,
159,167].
Fig. 2 Photomicrographs of
major harmful cyanobacterial
bloom groups, based on cellular
morphologies. abAggregated
single-cell coccoid genera,
including aMerismopedium
and bMicrocystis.cd,
filamentous, non-heterocystous
genera, including cOscillatoria
sp., dLyngbya sp. ef
Filamentous, heterocystous
genera, including eAnabaena
spp., and fNodularia sp.
H. W. Paerl, T. G. Otten
Many cyanobacterial genera readily exploit stratified con-
ditions by forming gas vesicles which provide buoyancy,
enabling them to maintain their position within the euphotic
zone and near the surface [59,120](Fig. 1). These surface
blooms maintain high rates of photosynthesis, even under
high ultraviolet radiation, while shading out underlying,
non-buoyant phytoplankton and macrophytes, thereby sup-
pressing their growth [58,60,160].
Cyanobacterial surface blooms may locally increase surface
water temperatures, due to light energy absorption via an array
of photosynthetic and photoprotective pigments (chlorophylls,
carotenoids, and phycobilins) [92,93]. Kahru et al. [66]used
remote sensing to demonstrate that cyanobacterial surface
blooms in the Baltic Sea could locally increase temperatures
by at least 1.5 °C above ambient waters. Likewise, Ibelings et
al. [61] showed that surface temperatures within cyanobacterial
blooms in Lake Ijsselmeer, Netherlands, were consistently
higher than surrounding surface waters. This represents a pos-
itive feedback mechanism by which cyanobacterial bloom
species can optimize their growth rates and provide competi-
tive dominance over eukaryotic phytoplankton.
Global warming also alters weather patterns and amounts
of precipitation, which may further enhance cyanobacterial
dominance. The frequency of extreme rainfall events is pro-
jected to increase [103]. This will lead to larger surface and
groundwater nutrient discharge events into water bodies.
Under conditions of excessive freshwater discharge, blooms
may be prevented by enhanced flushing; at least in the short
term. However, when the high discharge period subsides and
water residence time increases, the deposited terrestrial nutri-
ent load associated with these events can then be sequestered.
This scenario is particularly relevant during warm summer
months in large water bodies that have long water residence
times (i.e., large lake and reservoir systems, coastal lagoons
and semi-enclosed bays and sounds). Therefore, the settings
most likely to result in extreme cyanobacterial dominance are
predicted to begin with elevated winterspring rainfall and
runoff, followed by protracted periods of summer drought
where temperatures, vertical stratification, and water residence
times all increase simultaneously. Examples of this sequence
of events include the Swan River and Estuary (Australia),
Hartbeespoortdam (South Africa), the Neuse River Estuary
(North Carolina, USA), the Potomac River (Chesapeake Bay,
USA), and Lake Taihu (China) [98,105]. Attempts to
regulate discharge of rivers and lakes by dams and
sluices may increase residence time, and thus enhance
CyanoHAB proliferation.
Salinization, due to summer droughts, rising sea levels, and
increased use of freshwater for agricultural irrigation has in-
creased worldwide. Several common bloom-forming cyano-
bacterial genera are salt-tolerant, despite the fact that they are
most often found in freshwater systems. These include the N
2
fixers Anabaena,Anabaenopsis,Nodularia,andLyngbya,as
well as non-N
2
fixing genera,such as Microcystis [59,165,166]
and Oscillatoria. Some strains of Microcystis aeruginosa re-
main unaffected by salinities up to 10, which is 30 % of that of
seawater [7,148], and in Patos Lagoon, Brazil, it thrives under
mixohalineconditions [85]. Likewise, some Anabaena and
Anabaenopsis species can withstand salinities up to 15, while
toxic Nodularia spumigena can tolerate salinities exceeding 20
[81,84]. These salt-tolerant species are present in brackish
systems; presumably spurred on by a combination of nutrient
over-enrichment, climatic changes and salinization. Examples
of brackish systems prone to CyanoHAB events include: the
BalticSea(N.Europe),CaspianSea(W.Asia),SwanRiver
Estuary (Australia), San Francisco Bay (California, USA), and
Lake Ponchartrain (Louisiana, USA) [98,106].
0 5 10 15 20 25 30 35 40
Cyanobacteria
Temperature (oC)
% Maximum Growth Rate
Diatoms
Dinoflagellates
0
20
40
60
80
100
0
20
40
60
80
100
0
20
40
60
80
100
0
20
40
60
80
100
Chlorophytes
Fig. 3 Temperature dependence of the specific growth rates of three
eukaryotic phytoplankton classes and of CyanoHAB species common
in temperate freshwater and brackish environments. Data points are 5 °C
running bin averages of percent maximum growth rates from three to four
species within each class. Fitted lines are third-order polynomials and are
included to emphasize the shape of the growth versus temperature rela-
tionship. Percent maximum growth rates of individual species are pro-
vided in Paerl et al. [105]. Original data sources are [8,12,52,68,69,76,
120,150,173]
Harmful Cyanobacterial Blooms: Causes, Consequences, and Controls
The filamentous toxin-producing diazotroph
Cylindrospermopsis raciborskii, shows remarkable recent ex-
pansion of its geographical range. Cylindrospermopsis first
gained widescale attention following an outbreak of severe
hepatitis-like disease on Palm Island (Australia), the so-called
Palm Island mystery disease[14]. The outbreak occurred
after the local water supply was treated with copper
sulfate to control an algal bloom. A subsequent epidemiolog-
ical study confirmed the linkage between the mystery dis-
easeand the presence of Cylindrospermopsis [14]. Lysis of
the Cylindrospermopsis bloom released the highly stable toxin,
cylindrospermopsin, into the water supply.
Cylindrospermopsis was originally described as a tropi-
cal/subtropical genus [91]. However, C.raciborskii was
documented in Europe during the 1930s, and showed a
progressive colonization from Greece and Hungary towards
higher latitudes near the end of the twentieth century [91]. It
was described in France in 1994, in the Netherlands in 1999,
and it is now widespread in lakes in northern Germany [142,
167]. C.raciborskii was noted in Florida almost 35 years
ago, after which it aggressively proliferated throughout
lakes and rivers [16]. It is now commonly found throughout
the USA in reservoirs, lakes, rivers, and even oligohaline
estuarine waters experiencing various degrees of eutrophi-
cation and loss of water clarity [13,98]. C.raciborskii is
adapted to low light conditions typifying eutrophic waters, it
prefers water temperatures above 20 °C, and survives ad-
verse conditions using specialized vegetative resting cells
(akinetes) [91,142,167]. These bloom characteristics sug-
gest a link to eutrophication and global warming.
Recent studies have shown that the activation of akinetes in
the broadly distributed heterocystous species Aphanizomenon
ovalisporum is strongly temperature regulated [20]. Increases
in ambient temperatures may thereby play an important role in
the geographic dispersal strategy, and potential expansion of
this and other akinete-forming taxa.
Blooms of filamentous, non-heterocystous, toxin-
producing Lyngbya have become increasingly common and
problematic in nutrient-enriched freshwater and marine eco-
systems, including those that have experienced human distur-
bances such as: dredging, municipal waste inputs, and the
discharge of nutrient laden freshwater through coastal canals
[2,89,98,100,163]. Lyngbya is a ubiquitous genus, with
various species being found in both planktonic and benthic
habitats. L.majuscula (marine-benthic) and L.wollei (fresh-
water-benthic and planktonic) are opportunistic invaders.
Following large climatic and hydrologic perturbations such
as hurricanes, L.wollei is an aggressive initial colonizer of
flushed systems [98,106]. Lyngbya blooms can proliferate as
dense, attached or floating mats that shade other primary
producers, which enables Lyngbya to dominate the system
by effectively outcompeting them for light (Fig. 4). As is the
case with Cylindrospermopsis and Microcystis,this
CyanoHAB benefits from both human and climate-induced
environmental change.
Controls on Bloom Persistence and Collapse
Once a cyanobacterial bloom is established, it may persist for
months; even after nutrients (N and P) are reduced. Sediment
water column exchange of previously loaded, stored, and
recycled nutrients, as well as regeneration from cell turnover
and nutrient recycling by closely associated heterotrophic bac-
teria and microzooplankton grazers (e.g., protozoans and roti-
fers), can help sustain bloom biomass [94]. Key biotic factors
involved in bloom control include zooplankton (and possibly
benthic fauna and fish) grazing, bacterial interactions, and
viral lysis.
Cyanobacteria and Grazers
There is considerable debate as to how much influence zoo-
plankton grazers have on CyanoHABs [51,132,155]. There
is evidence that grazers in oligotrophic lakes exert a greater
impact on algae than those in eutrophic lakes [18]. This is
possibly due to increased phytoplankton productivity resulting
from nutrient-rich conditions, which allows the cells to simply
overwhelm any negative-grazing effects. Many CyanoHAB
genera also benefit by their tendencies to congregate as large
filamentous and colonial colonies, which reduces zooplankton
predation and interferes with the filtering capacity of bivalves.
Therefore, an overabundance of cyanobacteria relative to more
beneficial phytoplankton groups (e.g., diatoms) can negatively
affect natural populations of zooplankton fitness by their mor-
phology (size exclusion) [42], toxicity [25,43,44], or lack of
nutritional value [37,158].
Furthermore, ingestion of cyanobacteria by grazers does
not necessarily indicate that they are digested or assimilated.
Porter [112] showed that gelatinous algae were not digested
by Daphnia and that the cells could take up nutrients as they
passed through the animal
s gut. Van Donk et al. [153]found
that nutrient deficiency in phytoplankton led to their accumu-
lation of carbon and extra cellular compounds that could block
digestive enzymes in grazers. When cyanobacteria and other
phytoplankton are physiologically stressed by low nutrients,
they may increase their colony size to reduce grazing pressure.
Not only can they take up nutrients and remain viable through
zooplankton gut passage; they can also cause a decline in
zooplankter fitness due to malnutrition.
There is evidence that large cladocerans can control cya-
nobacterial blooms. Elser [34] reviewed the steps necessary
for cyanobacterial bloom formation. High nutrients favor all
phytoplankton, while nutrient stoichiometry and physical con-
ditions determine the potential for CyanoHAB formation. It is
H. W. Paerl, T. G. Otten
possible that large Daphnia species can control bloom initia-
tion if they are present in sufficient number before the bloom.
Even though the cladocerans may not be grazing significantly
on the cyanobacteria, the large numbers of grazers may still be
enough to suppress the bloom.
Occasionally, grazing can remove a substantial portion of
non-CyanoHAB blooms [131], but most often there is little to
no grazing influence on algal blooms [152]. Sellner et al. [132]
found that copepods reduced grazing on a river assemblage in
thepresenceofMicrocystis, although Bosmina seemed to in-
gest a significant amount of the bloom. Similarly, Leonard and
Paerl [72] found that Cylindrospermopsis blooms discouraged
copepod grazing, while rotifer grazing remained undeterred.
Both studies concluded that a large portion of the bloom
remained ungrazed.
Benthic mollusks have the potential to exert top down
control on phytoplankton abundance [87]. With regard to
cyanobacterial control, there are conflicting findings with
some reporting that mollusks, such as the zebra mussel
(Dreissena polymorpha), exhibit preferential (selective) graz-
ing of non-cyanobacterial phytoplankton [154] which leads to
increases in CyanoHAB abundance, whereas others report
that cyanobacteria are consumed indiscriminately [27].
Factors Initiating Bloom Collapse
Although grazers may restrict CyanoHAB expansion to
some degree, they generally are unable to keep pace with
an exponentially growing bloom [50]. However, blooms do
not last indefinitely and the cells comprising a bloom will
inevitably senesce and die, or enter a state of metabolic
dormancy; a phenomenon which occurs even in tropical
latitudes not prone to fall mixing events and cold temper-
atures. While there is always population turnover within a
bloom, there appears to be a tipping point at which once a
bloom begins to collapse, it does so rapidly (often within
days) [56]. This rapid collapse, and the subsequent de-
posit of large amounts of organic matter to the benthos,
can lead to hypoxia; a condition which can cause finfish
and shellfish kills and alter biogeochemical cycling [94,
97]. Physiological cues such as internal P-depletion may
prompt some cells to senesce and die while others
choose to enter a vegetative resting state [136,161].
Surface blooms may also disperse due to physical factors:
cooler temperatures, water column destratification, high tur-
bidity, and increased wind velocities which lead to mixing and
phytoplankton entrapment below the photic zone [5]; al-
though certain low-light adapted genera may be favored by
these conditions (e.g., Oscillatoria)[126]. The factors initiat-
ing apoptosis in cyanobacteria are poorly understood; al-
though similar to many types of cells a broad family of
proteases, known as caspases, are largely believed to drive
this process [3]. While there is some evidence for cyanobac-
terial control via predatory bacteria capable of secreting lysing
agents [118], the other major driver of cyanobacterial cell
death is likely viral lysis [145].
In general, viruses are ubiquitous in aquatic environments
and at concentrations upward of 10 million ml
1
,theyarethe
most abundant biological entity in the oceans [10,146]. The
majority of these viruses are bacteriophages, and with respect
to cyanobacteria, most of our knowledge of cyanophages has
come from marine environments [9]. Numerous studies have
demonstrated that cyanophages play an important, albeit poorly
understood, role in shaping phytoplankton abundance, commu-
nity structure, population succession, and on a larger scale,
Fig. 4 Benthic and mat-forming CyanoHABs. Left:Lyngbya confer-
voides covering a nearshore reef off Fort Lauderdale, FL (photo credit
K. Lane). Center:Lyngbya spp. mats covering the surface waters of
Ichetucknee Springs, FL. Right: blooms of Lyngbya sp. smothering
seagrass beds near Sanibel Island, coastal Gulf of Mexico, Florida (photo
credit H. Paerl)
Harmful Cyanobacterial Blooms: Causes, Consequences, and Controls
marine food webs. Studies have shown that the virus infection
frequency in cyanobacteria, based on visual detection, is 0.8
4.3 % of cells across diverse marine habitats [41], and that
similar percentages have been reported in freshwater bacteria
[80]. Since these numbers are based on visual observations of
cells with late-stage lytic infection, the true number of cells
infected is believed to be much higher.
In freshwater and estuarine systems, much less is known
about the extent to which viruses impact cyanobacteria, al-
though some in-roads have been made which suggest that these
cyanophages are likely equally as important as their marine
counterparts [168]. As of 2008, only 40 cyanophages had
been isolated from freshwaters [26], whereas isolated marine
cyanophages likely exceed this by at least 1 to 2 orders of
magnitude.
Many of the cyanophages isolated to date have exhibited
strain- or species-specific infectivity, although some isolates
have been found to infect hosts from multiple CyanoHAB
genera [26]. Numerous studies have corroborated that viral-
induced bacterial mortality is an important factor constrain-
ing and maintaining cyanobacterial abundances below their
environmental resource limited carrying capacities; and this
mortality may exceed the effect of zooplankton grazers,
especially in nutrient-rich waters [71,141]. Indeed, inves-
tigations of eutrophic freshwater lakes have often docu-
mented precipitous declines in CyanoHAB concentrations
concomitant with 10100-fold increases in cyanophage
abundance due to an average burst size of 20 to 50 virions
per host cell [169]. It has been estimated that viral lysis may
be responsible for up to 50 % of daily cyanobacterial cell
mortality [151]. High cell turnover may play a significant
role in bloom persistence due to the recycling of nutrients
from lysed cells [135]. Considering that the majority of
cyanotoxins remain intracellular, a sudden bloom collapse
has the potential to release large quantities of dissolved
toxins into the water column. Many of these toxins, such as
the cyclic heptapeptide microcystins and polycyclic cylin-
drospermopsin, are highly stable with half-lives on the order
of hours to weeks in natural settings depending on tempera-
ture, UV and the presence or absence of bacteria capable of
degrading these compounds [54](Table1). These com-
pounds may originate in inland lakes but can be transported
along the freshwatermarine continuum where they can ex-
ert their effects on marine flora and fauna. This scenario
occurred in Monterey Bay, CA (USA) when a microcystin-
producing CyanoHAB event in a nearby lake (Lake Pinto)
was flushed downriver and into the bay where the cells were
filtered by marine bivalves and subsequently consumed by
local sea otters. The result was that nearly two dozen sea
otters died of acute intoxication and subsequent analyses
identified that the microcystins bioaccumulated within the
shellfish meat at levels much higher than the ambient
concentration [82].
Transduction and Acquired Virulence
Cyanobacteria produce a wealth of seemingly nonessential
secondary metabolitesmany of which possess antibiotic,
toxic or siderophoric propertiesalthough most have not
been ascribed a function. One such group of secondary metab-
olites is the cyanotoxins (Table 1). While research to date has
failed to conclusively identify the true physiological or eco-
logical role of these compounds, they are known to exert
potent health effects on eukaryotic organisms, including
humans. Genetic analyses have determined that these gene
clusters are not highly constrained within certain groups, but
instead exhibit a patchy distribution across a variety of cya-
nobacterial genera [149]. Likewise, many cyanobacterial
strains contain multiple toxin operonsfor instance,
Oscillatoria sp. (PCC 6506) produces anatoxin-a,cylindro-
spermopsin and saxitoxin [116](Table1).
Phage-mediated gene transfer events are widely believed to
have played a significant role in microbial evolution and in
shaping the ecological niches these organisms exploit today
[41,109]. Advances in genomic sequencing have allowed
researchers to identify within cyanobacterial genomes the
genes of cyanophages; and conversely, cyanophage genomes
have been found to contain genes of cyanobacterial origin as
well [78]. Cyanophages are important agents of lateral gene
transfer [79,144]; although there is no conclusive evidence
that cyanotoxin genes are actively exchanged with other spe-
cies or genera. However, there is compelling evidence to
believe that parts of the microcystin synthetase operon (mcy)
have undergone horizontal gene transfer events in the past
[147,175]. As such, it is hazardous to assume a given genus or
species will always be nontoxic without verification by bio-
chemical or molecular analysis.
Managing Cyanotoxins
Eutrophic waters are often reported to contain high concentra-
tions of cyanotoxins, a phenomenon likely attributable to the
high concentration of cyanobacteria supported by abundant
nutrients [90]. The cues for toxin synthesis are likely subject
to multiple environmental and cellular factors acting in unre-
solved synergistic or antagonistic combinations [55,86,176].
The effect that cell density has on cellular toxin quota has not
been adequately resolved due to contradictory reports [65,
170], although cells in exponential growth phase are reported
to produce more microcystin than when in lag or stationary
phase [162]. Cyanobacterial concentrations are often positively
correlated with microcystins at a range of low and high cell
densities because the intracellular toxin contents remain rela-
tively balanced due to losses to daughter cells during periods of
division [77]. An investigation of 22 Canadian lakes spanning
from low to high trophic states identified toxic cyanobacteria in
H. W. Paerl, T. G. Otten
all systems and observed increasing microcystin concentrations
as trophy increased [48]. In that study, the authors identified
total nitrogen (TN) as the best predictor of total microcystin,
with increasing TN correlating with increased microcystins.
The observation that increased concentrations of dissolved
macronutrients, N and/or P, favors growth of toxigenic cyano-
bacteria and toxin production is routinely reported [29]; how-
ever, this is likely a function of increased cell concentrations as
opposed to surplus N or P actually promoting toxin gene
expression. In fact, from a molecular basis, increased N should
result in decreased microcystin biosynthesis owing to multiple
transcription factor binding sites for the global nitrogen regu-
lator (NtcA) within the mcy promoter which lead to upregula-
tion of toxin biosynthesis under nitrogen-limiting conditions
[49,174]. Likewise, there is a growing body of evidence that
suggests microcystin transcription may be dual controlled by
iron availability via the Fur family of transcriptional regulators
[1,133]. However, both of these groups of regulators may
ultimately be controlled by the redox status of the cell [176].
Finally, for reasons unclear, warmer temperatures appear to
favor the growth of toxigenic strains of Microcystis over non-
toxic ecotypes [24,30]; a troubling trend considering projec-
tions of future climate scenarios.
Cyanotoxins in drinking water reservoirs represent a potent
human health threat on a global scale which to date has not
been adequately managed from a public health perspective.
The potential for physical transport and trophic transfer
(biomagnification) from freshwater environments to marine
ecosystems further increases exposure risks in environments
not routinely screened for cyanotoxins. One of the reasons for
the lack of broadscale regulation has been the lag between
identifying these harmful metabolites and the subsequent years
of toxicological and epidemiological studies required to fully
characterize these risks. The other major hurdle facing
CyanoHAB monitoring is the lack of standardized analytical
tests to detect and quantify cyanotoxins. However, as more of
these harmful compounds are discovered in cyanobacteria
(e.g., BMAA, jamaicamides, aeruginosins, etc.), the more
cumbersome their management will become [22,31,62]. For
this reason, it makes more sense to address cyanotoxin man-
agement from a broader perspective. There is little reason not
to manage CyanoHABs in a similar manner that Escherichia
coli is currently managed; which is to say, on a presence/
absence context in finished drinking waters and on a concen-
tration basis (CFU per milliliter) in raw waters. Under this
framework, management decisions are not based on serotyping
an E.coli strain to determine its pathogenicity, instead its
presence and/or abundance dictate what subsequent actions
are required. Raw waters containing cyanobacteria could like-
wise be managed based on their cell concentrations. For brack-
ish and/or freshwater cyanobacteria, there are at least 20
common bloom-forming genera that are known to produce
cyanotoxins (Table 1). While species differences may exist
with regard to their toxigenicity, the potential for toxin gene
acquisition via transduction or other lateral gene transfer event
in routinely nontoxic species cannot be overlooked; which is
why management decisions should be based at the genus level.
This approach would remove much of the subjectivity inherent
to microscopic identification of morphologically plastic cya-
nobacteriaa considerable problem when attempting to char-
acterize cyanobacteria down to the species level.
Research over the past two decades on microcystin-
producing genera has demonstrated that in most cases the
majority of cyanobacterial cells in a bloom are nontoxigenic
[70]. While this level of insight is generally lacking at present
for the other cyanotoxins, the patchy distribution of cyano-
bacterial toxin genes makes informed bloom management
difficult without specialized equipment to directly measure
for these genetic markers and/or their analytes. In an attempt
to simplify CyanoHAB management, the World Health
Organization (WHO) has issued provisional guidance for both
drinking and recreational waters for the most ubiquitous cya-
notoxin, microcystin (MC-LR), based on general metrics of
cyanobacterial abundance such as chlorophyll-aand cell
counts [171]. Figure 5displays the recommended WHO
guidelines for recreational exposure to microcystins and
assumes a conservative, low risk of adverse health effect at
4μgl
1
, although the WHO acknowledges exposures up to
10 μgl
1
are likely to be relatively low risk; exposures be-
tween 10 and 20 μgl
1
are considered moderate risks and
anything above 20 μgl
1
carries a high risk of adverse health
effects. The data from Fig. 5were adapted from three previous
studies comparing microcystin-producing cyanobacterial
(predominantly Microcystis spp., but also some Anabaena
spp.) cell densities with microcystin concentrations from three
distinct lake types and trophic states (Western Lake Erie, OH:
mesotrophic; Missisquoi BayLake Champlain,VT: eutro-
phic; and Zhushan and Meiliang BaysLake Taihu, China:
hypertrophic). All samples were collected over two or three
summer periods, non-detects and samples below the limits of
detection were omitted and detailed information about these
studies is described elsewhere [90,121,125]. Note that in the
Lake Erie study microcystin-LR was measured by protein
phosphatase 2A assay (PP2A) instead of enzyme-linked im-
munosorbent assay (ELISA) as was used in the other studies;
although these methods have been shown to yield comparable
results [117]. In this example, some samples that contained
low cell concentrations exceeded the amount of toxin
expected, although this only occurred in the higher trophic
lakes (Lake Champlain and Lake Taihu). Most importantly,
however, was that the WHO provisional guidelines adequate-
ly predicted maximal microcystin concentrations; with no
samples containing less than 10
6
cells ml
1
exceeding the
moderate risk level for microcystin (20 μgl
1
). This figure
represents a simplified meta-analysis of the type of large-scale
analyses encompassing all aquatic trophic states that will be
Harmful Cyanobacterial Blooms: Causes, Consequences, and Controls
needed to characterize the exposure risks for all microcystins
and the numerous other cyanotoxins endemic in many water-
bodies worldwide. An extensive compilation of CyanoHAB
events from around the world in which standardized measure-
ments and units were utilized (e.g., micrograms of toxin per
liter and cells per milliliter) would frame realistic toxin con-
centrations produced by these genera under natural settings in
which management decisions could be based on broad, simple
metrics such as cell concentration. For most cyanotoxins,
these data likely already exist due to myriad studies over the
years on cyanobacteria around the globe; although currently
there is no central repository in which to store and view this
information. The creation of a widely advertised, internet
accessible database has the potential to make this a reality.
Controlling CyanoHABs in Aquatic Ecosystems
The combination of anthropogenic nutrient loading, rising
temperatures, enhanced vertical stratification, increased res-
idence time and salination will favor cyanobacterial domi-
nance and CyanoHAB proliferation in a wide range of
aquatic ecosystems (Fig. 6). The recent geographic expan-
sion, and in some cases intensification, of CyanoHABs has
serious consequences for human water supplies, fisheries,
and recreational resources.
Nutrient input reductions are the most obvious targets
which can be altered and as such should be a central part of
any CyanoHAB mitigation strategies in both freshwater and
marine environments (Fig. 6). We have long been aware that P
input reduction is an effective means of reducing cyanobacte-
rial dominance in aquatic, and especially freshwater, ecosys-
tems. However, there are numerous and increasing instances
where N input reductions are also needed. This is especially
the case in eutrophic, CyanoHAB susceptible lakes, rivers,
estuaries, and coastal waters which are capable of assimilating
more N and increasing their trophic state [104]. A key man-
agement priority is to establish N and P input thresholds (e.g.,
TMDLs), below which CyanoHABs can be controlled in
terms of magnitude, temporal and spatial coverage. The ratios
of N to P inputs should be considered when developing these
thresholds. Ideal input ratios are those that do not favor
specific CyanoHAB taxa over others, but there does not
appear to be a universal ratioabove or belowwhich
CyanoHABs can be consistently and reliably controlled. For
this reason, total nutrient loads and concentrations need to be
considered in CyanoHAB management [73,74]. For example,
it is generally thought that total molar N:P ratios above 15
discourage CyanoHAB dominance [137]. However, if the
nutrient load and internal concentrations of N and/or P are
extremely high, a ratio approach for reducing CyanoHABs is
notlikelytobeeffective[105,106,172].
There are many ways to reduce nutrient inputs on a lake or
larger ecosystem scale. Nutrient inputs have been classified as
point source and non-point source. Point sources are often
associated with well-defined and identifiable discharge sites;
therefore, these nutrient inputs are relatively easy to control. It
is therefore no surprise to see that most of the short-term
successes in nutrient input control are those associated with
point sources, including wastewater treatment plant, industrial
effluent, and other distinct input sources. The major challenge
that remains in many watersheds is targeting and controlling
nonpoint sources, which in many instances are the largest
sources of nutrients; hence, their controls are likely to play a
critical role in mitigating CyanoHABs.
Nutrient management strategies may also include the
removal of nutrients from receiving waters after they have
been discharged. Examples of post-discharge removal
Fig. 5 Comparison of
CyanoHAB cell concentrations
and microcystin-LR from
mesotrophic (Western Lake
Erie, OH, USA [121]),
eutrophic (Missiquoi Bay, Lake
Champlain, VT, USA [125])
and hypertrophic (Meiliang and
Zhushan Bays, Lake Taihu,
Jiangsu, China [90]) waters. The
WorldHealthOrganizations
(WHO) provisional guidelines
for microcystin exposure in rec-
reational waters [171] is included
to illustrate how health alert
levels could be based on simple
water quality metrics such as
CyanoHAB cell density
H. W. Paerl, T. G. Otten
which have been attempted include: dredging sediments,
harvesting macrophytes that have assimilated nutrients,
and in some cases stocking and then removing higher tro-
phic level consumers (finfish and shellfish) to eliminate
nutrient-containing biomass. Other approaches have in-
volved precipitating, binding, and immobilizing nutrients
in the sediments [53,123]. All the above techniques have
been variably effective [105], and in some cases, the results
were even counterproductive. For example, sediment dredg-
ing can disrupt important biogeochemical processes in the
surface sediments and benthos (e.g., denitrification), and it
can lead to enhanced mobilization of previously retained
nutrients. Also, disturbance of the sediment meso- and
micro-fauna, as well as microbial communities, can disrupt
nutrient, oxygen, and carbon cycling to the detriment of the
ecosystems undergoing mitigation and restoration [138].
Manipulating physical factors that are known to play key
roles in CyanoHAB competition versus other eukaryotic
phytoplankton can, at times and under specific conditions,
have some beneficial effects on water bodies plagued with
CyanoHABs. Vertical mixing devices, bubblers, and other
means of breaking down destratification have proven effec-
tive in controlling outbreaks and persistence of CyanoHABs
in relatively small impoundments [59,156]. Generally, these
devices have limited applicability in large lake, estuarine,
and coastal waters because they simply cannot exert their
forces over such large areas and volumes. Increasing the
flushing rates, and thereby decreasing water residence time,
can be effective in reducing or controlling CyanoHABs [11,
83,105]. However, care must be taken to make sure that the
flushing water is relatively low in nutrient content, so as not
to compound the enrichment problem. Furthermore, few
catchments have the luxury of being able to use precious
water resources normally reserved for drinking or irrigation
for flushing purposes. This is especially true of regions
where freshwater runoff is limited and/or is periodically
impacted by droughts [124].
Lastly, flushing can alter the circulation regimes of re-
ceiving water bodies [114]. Care must be taken not to alter
the physical environment in such a way (e.g., increasing
thermal or chemical density stratification, entrainment bays
and arms of water bodies) so that CyanoHABs are trapped
in, rather than flushed out, of the system [114].
In a great majority of cases, nutrient input reductions are
the most direct, simple, and ecologically/economically feasi-
ble CyanoHAB management strategy. Nutrient input reduc-
tions that are aimed at specifically reducing CyanoHAB
competitive abilities, possibly combined with physical con-
trols (in systems that are amenable to those controls) are often
the most effective strategies. Nutrient (specifically N) treat-
ment costs can be prohibitive, in which case, alternative
nutrient removal strategies may be called for. These would
Positive
• High P (High N for some)
• Low N (DIN, DON) (only
applies to N
2
fixers)
• Low N:P Ratios
• Low turbulence
• Low water flushing-Long
water residence time
• High (adequate) light
• Warm temperatures
• High dissolved organic
matter
• Sufficient Fe (+ trace
metals)
• Low grazing rates
Negative
• High DIN/ total N (only
applies to N
2
fixers)
• Low P (DIP)
• High N:P ratios
• High turbulence & vertical
mixing
• High water flushing-Short
water residence time
• Low light (for most taxa)
• Cool temperatures
• Low dissolved organic
matter
• Low Fe (+ trace metals)
• High grazing rates
• Viruses (cyanophages)
• Predatory bacteria
Cyanos
Rates
Rates
Diversity
Modulating factors
• Strong biogeochemical gradients (e.g.
persistent stratification, stable benthos)
• Heterogeneous and diverse habitats (e.g.
reefs, seagrasses, marshes, sediments,
aggregates)
• Selective grazing
• “Toxin” production??
Environmental factors controlling CyanoHABs
Fig. 6 Suite of positive and negative effectors as well as modifying environmental and ecological factors that influence CyanoHAB potentials in
aquatic ecosystems
Harmful Cyanobacterial Blooms: Causes, Consequences, and Controls
include construction of wetlands, cultivation and stimulation
of macrophytes, stocking of herbivorous (and specifically
cyanobacteria consuming) fish and shellfish species [63].
Overall, in addition to nutrient input reductions, water
managers will have to accommodate the hydrological and
physicalchemical effects of climatic change in their strate-
gies. Without curbing greenhouse gas emissions, future warm-
ing trends and their impacts on aquatic ecosystems will likely
only lead to further expansion and dominance of aquatic
ecosystems by these nuisance species.
Acknowledgments We thank A. Joyner and N. Hall for technical
assistance and J. Huisman, J. Dyble Bressie, P. Moisander, and V. Paul
for contributions and helpful discussions. This work was supported by the
National Science Foundation (OCE 07269989, 0812913, 0825466, and
CBET 0826819, 1230543, and Dimensions of Biodiversity 1240851),
U.S. EPA-STAR project R82867701, and the NOAA/EPA-ECOHAB
project NA05NOS4781194, the North Carolina Sea Grant Program
R/MER-47, and California Delta Stewardship Council project 2044.
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H. W. Paerl, T. G. Otten
... CyanoHABs are caused by toxin-producing photosynthetic prokaryotes called cyanobacteria and are characterised by scums that can be green, bright blue, or other colours on the surface of brackish and freshwater. In cya-noHABs, typically one or two cyanobacterial species dominate the community [4,5], with major harmful genera being Microcystis, Nodularia, Dolichospermum, Oscillatoria, Aphanizomenon, and Phormidium [6]. In marine environments, these blooms are referred to as harmful algal blooms (HABs), dominated by toxic algal species and non-cyanobacterial species, such as those of the dinoflagellates and diatoms, resulting in fish, bird, and marine mammal mortality in extreme cases [7]. ...
... The functional role of cyanotoxins is largely unknown; however, some studies suggest they may act as a chemical defence or physiological aide for cyanobacteria [8][9][10]. Cyanobacterial blooms can be harmful in a number of ways, such as by outcompeting phytoplankton, depleting oxygen, and producing cyanotoxins within the environment, killing fish and inhibiting plant growth in the process [4]. The most common toxins found in cyanoHABs include microcystins [11] and nodularins [12], which are hepatotoxins inhibiting protein phosphatase, and neurotoxins such as anatoxin-a [13], guanitoxin [14], 2,4-diaminobutyric acid (DAB) [15], and acute effects of ß-methylamino-L-alanine (BMAA) [16], which inhibit neuronal function. ...
... Although BMAA is labelled as a neurotoxin here, the chronic effects have been long debated [17][18][19][20][21]. These toxins threaten human health through the consumption of contaminated fish, molluscs, and gastropods, as well as coming into contact with bloom material during recreational water activities [4]. Whilst the threat of cyanotoxins to human and domestic animal health is not fully understood, resources and interest are invested in understanding public and domestic animal health risks. ...
Article
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Global warming and over-enrichment of freshwater systems have led to an increase in harmful cyanobacterial blooms (cyanoHABs), affecting human and animal health. The aim of this systematic map was to detail the current literature surrounding cyanotoxin poisonings in terrestrial wildlife and identify possible improvements to reports of morbidity and mortality from cyanotoxins. A systematic search was conducted using the electronic databases Scopus and Web of Science, yielding 5059 published studies identifying 45 separate case reports of wildlife poisonings from North America, Africa, Europe, and Asia. Currently, no gold standard for the diagnosis of cyanotoxin intoxication exists for wildlife, and we present suggested guidelines here. These involved immunoassays and analytical chemistry techniques to identify the toxin involved, PCR to identify the cyanobacterial species involved, and evidence of ingestion or exposure to cyanotoxins in the animals affected. Of the 45 cases, our recommended methods concurred with 48.9% of cases. Most often, cases were investigated after a mortality event had already occurred, and where mitigation was implemented, only three cases were successful in their efforts. Notably, only one case of invasive cyanobacteria was recorded in this review despite invasive species being known to occur throughout the globe; this could explain the underreporting of invasive cyanobacteria. This systematic map highlights the perceived absence of robust detection, surveillance, and diagnosis of cyanotoxin poisoning in wildlife. It may be true that wildlife is less susceptible to these poisoning events; however, the true rates of poisoning are likely much more than is reported in the literature.
... As a result, phytoplankton community composition and biomass are often used as indicators for characterizing the ecological status of lakes. In recent decades, blooms of phytoplankton in lakes that are caused by atypical proliferation and a rapid increase in algal biomass of dominant species have become increasingly common, garnering worldwide attention (Guo 2007;Huo et al. 2021;Paerl et al. 2011;Paerl and Otten 2013;Schindler et al. 2012). These blooms have the potential to significantly and negatively impact water quality (e.g., decreasing transparency, producing taste and odor compounds, and inducing hypoxia and anoxia by the degradation of senescent blooms) (Scheffer et al. 1993;Paerl and Otten 2013;Izaguirre and Taylor 2004), human use of the ecosystem (e.g., interrupting water supply, disrupting tourism and fisheries, and causing losses in fish cultures), and human health (e.g., through the production of biotoxins) (Davidsona et al. 2012). ...
... In recent decades, blooms of phytoplankton in lakes that are caused by atypical proliferation and a rapid increase in algal biomass of dominant species have become increasingly common, garnering worldwide attention (Guo 2007;Huo et al. 2021;Paerl et al. 2011;Paerl and Otten 2013;Schindler et al. 2012). These blooms have the potential to significantly and negatively impact water quality (e.g., decreasing transparency, producing taste and odor compounds, and inducing hypoxia and anoxia by the degradation of senescent blooms) (Scheffer et al. 1993;Paerl and Otten 2013;Izaguirre and Taylor 2004), human use of the ecosystem (e.g., interrupting water supply, disrupting tourism and fisheries, and causing losses in fish cultures), and human health (e.g., through the production of biotoxins) (Davidsona et al. 2012). Controlling algal blooms has become a primary concern in lake management and restoration. ...
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Gaining a deeper understanding of factors that influence changes in phytoplankton community has significant implications for shallow lake management. The present study examined changes in the algae community of three shallow eutrophic lakes of the Taoge water system between 2008 and 2018 and the related factors influencing these changes. The composition of the algal community varied significantly during this period with the relative diatom biomass in lakes Changdanghu and Gehu increasing between 2014 and 2016 and again decreasing after 2017. However, relative cyanobacteria biomass initially decreased and later increased; meanwhile, the proportion of biomass of other phyla decreased continuously in the study period. Lake Zhushanhu showed similar trends, although it eventually returned to its initial state with absolute Microcystis dominance. Furthermore, the analysis of driving factors revealed that the concentrations of total nitrogen (TN), nitrate (NO3), and orthophosphate (PO4) were significantly associated with a significant increase in Microcystis biomass. Meteorological conditions also influenced changes in total algal and diatom biomasses, which were inversely related to the daily mean and daily maximum wind speeds. Monthly cumulative precipitation was only significantly associated with diatom biomass. Meanwhile, rainfall primarily affected the algal community structure between 2013 and 2017; an increase in the relative biomass of diatoms coincided with increased precipitation. Coordinating nitrogen and phosphorous use within the Taoge water system should improve lake habitat management; a broader perspective in attempts to control global and regional climate change may be needed.
... Cyanobacterial blooms have many negative effects. Cyanobacteria blooms reduce the water surface clarity and thus inhibit the growth of aquatic macrophytes; cyanobacterial blooms reduce the dissolved oxygen content of water, resulting in the death of aquatic organisms, including fish, crab, shrimp, etc. [2]. Furthermore, cyanobacterial blooms make water toxic, as many cyanobacteria produce highly toxic secondary metabolites known as "cyanotoxin". ...
... Temperature, pH, UV, and chloroform sensitivity assessment were performed. Aliquots of cyanophage stock solution (2.8 × 10 5 PFU/mL) were adjusted to different pH (2,3,4,5,6,7,8,9,10,11,12) with NaOH or HCl, in triplicates and incubated for 2 h at 25 • C; aliquots of cyanophage stock solution (2.8 × 10 5 PFU/mL) were incubated at 0 • C, 25 • C, 40 • C, 60 • C, and 80 • C, respectively, in triplicates. Samples were collected at 0 min, 20 min, 40 min, 60 min, 80 min, 100 min, and 120 min, respectively; aliquots of cyanophage stock solutions were irradiated under UV lamp (253.7 nm) in triplicates. ...
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Microcystis aeruginosa is a major harmful cyanobacterium causing water bloom worldwide. Cyanophage has been proposed as a promising tool for cyanobacterial bloom. In this study, M. aeruginosa FACHB-1326 was used as an indicator host to isolate cyanophage from Lake Taihu. The isolated Microcystis cyanophage Mae-Yong1326-1 has an elliptical head of about 47 nm in diameter and a slender flexible tail of about 340 nm in length. Mae-Yong1326-1 could lyse cyanobacterial strains across three orders (Chroococcales, Nostocales, and Oscillatoriales) in the host range experiments. Mae-Yong1326-1 was stable in stability tests, maintaining high titers at 0–40 °C and at a wide pH range of 3–12. Mae-Yong 1326-1 has a burst size of 329 PFU/cell, which is much larger than the reported Microcystis cyanophages so far. The complete genome of Mae-Yong1326-1 is a double-stranded DNA of 48, 822 bp, with a G + C content of 71.80% and long direct terminal repeats (DTR) of 366 bp, containing 57 predicted ORFs. No Mae-Yong1326-1 ORF was found to be associated with virulence factor or antibiotic resistance. PASC scanning illustrated that the highest nucleotide sequence similarity between Mae-Yong1326-1 and all known phages in databases was only 17.75%, less than 70% (the threshold to define a genus), which indicates that Mae-Yong1326-1 belongs to an unknown new genus. In the proteomic tree based on genome-wide sequence similarities, Mae-Yong1326-1 distantly clusters with three unclassified Microcystis cyanophages (MinS1, Mwe-Yong1112-1, and Mwes-Yong2). These four Microcystis cyanophages form a monophyletic clade, which separates at a node from the other clade formed by two independent families (Zierdtviridae and Orlajensenviridae) of Caudoviricetes class. We propose to establish a new family to harbor the Microcystis cyanophages Mae-Yong1326-1, MinS1, Mwe-Yong1112-1, and Mwes-Yong2. This study enriched the understanding of freshwater cyanophages.
... Due to climate warming and anthropogenic eutrophication, occurrences of cyanobacterial blooms (CYBs) have been increasing in frequency and have become a growing major problem in freshwater ecosystems (Paerl and Otten 2013). And research has shown that increasing water temperature favors the bloom of toxin-producing cyanobacteria, such as Microcystis, Anabaena, Oscillatoria, and Nostoc spp. ...
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As filter-feeders, bivalves naturally come into direct contact with microcystins (MCs) in eutrophic water bodies suffering from cyanobacteria blooms. To date, however, no studies have quantified the dynamics of microcystin accumulation and depuration in the edible freshwater bivalve Corbicula fluminea when exposed to dense bloom concentrations of Microcystis aeruginosa, while considering dynamic changes of biochemical indexes and feeding structure. In the present study, the bioaccumulation and detoxification of microcystin-LR (MC-LR) in C. fluminea were investigated. Our results showed that C. fluminea would graze equally efficiently on green algae and M. aeruginosa, irrespective of whether the M. aeruginosa strains were toxic or non-toxic. MCs could be accumulated and depurated by C. fluminea efficiently. In addition, linear and exposure time-dependent MC-LR accumulation patterns were observed in C. fluminea. Activities of biotransformation (glutathione S-transferase, GST) and antioxidant enzymes (superoxide dismutase, SOD, and catalase, CAT) and malondialdehyde (MDA) contents in various tissues of treated clams were stimulated by MCs in a tissue-specific manner. Our findings indicated that C. fluminea hepatopancreas was the primary target organ for MC-LR detoxification processes, as evidenced by a significant increase in GST activity. Besides, gills and mantle were more sensitive than the other tissues to oxidative stress in the initial microcystin exposure period with a significant increase in SOD activity. The scanning electron microscopy (SEM) observations revealed that the lateral cilia in the gill aperture were well developed during the MCs exposure period, which could perform the filter-feeding function instead of the damaged frontal cilium. This study provides insight into the possible tolerance of C. fluminea exposed to dense bloom concentrations of M. aeruginosa.
... Water eutrophication is widespread throughout the world, resulting in the 38 proliferation of algae in the water, forming harmful blooms, and causing water 39 pollution [1,2]. Bloom-forming cyanobacterial taxa can be harmful to environmental, 40 organismal, and human health [3]. Its large-scale outbreaks will reduce the dissolved 41 oxygen content in the water, affecting the normal growth of aquatic organisms, and 42 breaking the stability and balance of the ecosystem [4]. ...
Preprint
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To avoid the disadvantage that artemisinin granules coated with millimeter level chitosan alginate are easy to settle and improve the dispersion of granules in water, improved artemisinin sustained release granules (ASGs) were prepared by ultrasonic technology combined with ion crosslinking method in this study. The release kinetics of two kinds of granules under different media conditions (temperature, ionic strength, pH, algal liquid, and Taihu Lake water) were studied. The physicochemical characterization showed that the diameter and zeta potential of the improved ASGs were 1189.5nm and -38.0mV, respectively. Here, the drug release of chitosan-coated artemisinin alginate granules is affected by the temperature, pH, and ionic strength of the release medium. Whether ASGs or improved ASGs, drug release increased with the increase of temperature and ionic strength, but decreased with the increase of pH. More importantly, the release kinetics study showed that the release mechanism of the improved ASGs in Taihu Lake water and algae liquid is matrix dissolution, while the release of ASGs in Taihu Lake water was controlled by diffusion and skeleton dissolution. The growth experiment of cyanobacteria showed that the improved ASGs have a long-term inhibitory effect on algae cells, and the inhibitory effect on cyanobacteria increased with the increase of dosing concentration. Our study clearly shows that the granules with reduced diameter have the characteristics of rapid dispersion and continuous release, and have the potential to be applied to the control of cyanobacteria bloom.
... This combination of perturbations could be particularly potent in generating reactive algal response as algal growth begins anew at the beginning of the next growing season. There could be important practical bene ts in better understanding environmental drivers of such reactive nutrient-driven algal blooms, since the frequency and magnitude of harmful algal blooms is thought to have increased in recent years (Michalak et al. 2013, Paerl andOtten 2013). This increasing trend is pronounced in global datasets for large lakes (Ho et al. 2019), although data for smaller lakes in North America show little trend over a 10-year period spanning the beginning of the 21 st century (Wilkinson et al. 2021). ...
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Algal blooms are typical of many aquatic freshwater ecosystems in seasonal environments. Such blooms could derive from transient reactive dynamics of algae and limiting nutrients following seasonal perturbation events. Linking parameter estimates derived from previously published lab experiments with empirical estimates of algal density-dependence, we modeled dynamic interactions between nutrients and the green algal species Chlorella vulgaris and tested model predictions in a dozen 140L mesocosms supplied with biweekly inputs of liquid fertilizer. Consistent with the reactive nutrient-driven model, Chlorella populations exhibited an initial surge in abundance over the first month followed by collapse as they rapidly converged on stable equilibria. The reactive model suggests that the magnitude of transient blooms is positively related to augmentation of nutrients and depression of algae over the winter period. The magnitude of both algal peaks and equilibrium abundance was positively related to fertilizer loading, as predicted by the reactive model. Our results suggest that transient reactive responses to climate-driven perturbation events can be an important contributor to seasonal algal blooms observed in many temperate freshwater ecosystems. Controlled experimental studies such as ours may be helpful in understanding and potentially mediating the impact of fertilizer runoff on freshwater systems in temperate agricultural landscapes.
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Algal blooms are severe ecological disasters in the marine environment, affecting the biogeochemical cycles substantially. It is critical to explore how the prokaryotic community responds to the dynamics of algal blooms in the marine environment. The shifts in prokaryotic communities during the algal blooms have been extensively investigated, while the interactions and assembly mechanisms of prokaryotic communities are still incompletely understood. We conducted nutrient addition cultivations for the brackish water from the Pearl River estuary to simulate the algal bloom process and monitored the prokaryotic community compositions over forty days. Results showed evident differences between blooming and after-bloom stages of prokaryotic communities in diversity and taxonomic compositions. Bacillus , Gimesiaceae, and Fibrobacteraceae were dominant before the cultivation. Mesoflavibacter , Rhodobacteraceae, and Acinetobacter were accumulated in the blooming stage. Acinetobacter , Comamonadaceae, and Gimesia were enriched in the after-blooming stage, while Mesoflavibacter, Rhodobacteraceae, and Acinetobacter were active during the whole blooming period. Co-occurrence networks analysis showed that prokaryotic interactions were predominantly driven by positive relationships that impacted the algal blooming fates. Rhodobacteraceae, Flavobacteriaceae, Winogradskyella, and Pseudomonas are the keystone groups of the prokaryotic communities in the blooming stage network, while Marinobacter, Thalassobaculum, Actinobacteria, Flavobacterium, and Rhodobacteraceae are the keystone groups of the after-bloom stage network. Functional prediction by FAPROTAX showed that dissimilatory nitrate reduction increased in the after-bloom stage. Our study revealed the dynamic of the prokaryotic communities and the characteristics of their co-occurrent profiles, which shed light on revealing the potential functions of prokaryotic behaviors during estuarine algal blooming events.
Article
The harmful algal bloom (HAB) issue is intensifying and affecting water supplies around the world. The cell-free supernatant (CFS) of algicidal bacteria has been extensively used for HAB control. However, the remaining nutrients in the water may cause the HAB species to bloom again. In this study, we used the CFS of Bacillus sp. AK3 obtained from nutrient broth medium (NB-CFS) and M9 minimal medium (M9-CFS), to eradicate HAB species. Based on extracellular metabolomics data, seven antimicrobial compounds, i.e., cyclo (leu-pro), cyclo (phe-pro), norharman, trans-3-indoleacrylic acid, hypoxanthine, kanosamine, and betaine, were detected in both NB-CFS and M9-CFS, albeit at different intensities. In the treatment of HAB water, NB-CFS and M9-CFS exhibited strong Microcystis and Pseudanabaena (harmful cyanobacteria) growth inhibition, whereas Chlorella (green algae) growth was promoted, indicating a specific inhibitory effect of CFS. The TP, TN, and COD levels in the water significantly increased after adding both CFSs. Interestingly, NB-CFS proved superior in promoting the beneficial Chlorella species, which can completely remove TP (100%) and effectively reduce TN and COD in HAB water at the end of the experiment. The combination of species-specific algicidal compounds with Chlorella may be a feasible strategy for the simultaneous elimination of HAB species and nutrients from water.
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Billions of years ago, the Earth's waters were dominated by cyanobacteria. These microbes amassed to such formidable numbers, they ushered in a new era—starting with the Great Oxidation Event—fuelled by oxygenic photosynthesis. Throughout the following eon, cyanobacteria ceded portions of their global aerobic power to new photoautotrophs with the rise of eukaryotes (i.e. algae and higher plants), which co‐existed with cyanobacteria in aquatic ecosystems. Yet while cyanobacteria's ecological success story is one of the most notorious within our planet's biogeochemical history, scientists to this day still seek to unlock the secrets of their triumph. Now, the Anthropocene has ushered in a new era fuelled by excessive nutrient inputs and greenhouse gas emissions, which are again reshaping the Earth's biomes. In response, we are experiencing an increase in global cyanobacterial bloom distribution, duration, and frequency, leading to unbalanced, and in many instances degraded, ecosystems. A critical component of the cyanobacterial resurgence is the freshwater‐marine continuum: which serves to transport blooms, and the toxins they produce, on the premise that “water flows downhill”. Here, we identify drivers contributing to the cyanobacterial comeback and discuss future implications in the context of environmental and human health along the aquatic continuum. This Minireview addresses the overlooked problem of the freshwater to marine continuum and the effects of nutrients and toxic cyanobacterial blooms moving along these waters. Marine and freshwater research have historically been conducted in isolation and independently of one another. Yet, this approach fails to account for the interchangeable transit of nutrients and biology through and between these freshwater and marine systems, a phenomenon that is becoming a major problem around the globe. This Minireview highlights what we know and the challenges that lie ahead.
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Fucoxanthin (Fx) has attracted great interest due to its remarkable biological activities such as antioxidant and anti-obesity, and its increasing demands in biopharmaceutical and cosmetic fields. However, its commercial production is limited by low yield and high cost. In this study, we isolated and identified a species of golden algae (Ochromonas sp.) capable of engulfing Microcystis aeruginosa (M. aeruginosa) and accumulating Fx. After 72 h mixotrophic cultivation of Ochromonas sp. and M. aeruginosa, the algal culture changed from green to yellow-brown, and the content of Fx and the daily production rate were up to 11.58 mg g⁻¹, and 1.315 mg L⁻¹ d⁻¹, respectively. The utilization rate of M. aeruginosa was 527.27 fg cell⁻¹. This study will not only provide a new thought to produce Fx in an efficient, low-cost, and sustainable way but an innovative method for the control and treatment of harmful cyanobacterial blooms from eutrophic freshwaters as well.
Book
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Cyanobacteria make a major contribution to world photosynthesis and nitrogen fixation, but are also notorious for causing nuisances such as dense and often toxic `blooms' in lakes and the ocean. The Ecology of Cyanobacteria: Their Diversity in Time and Space is the first book to focus solely on ecological aspects of these organisms. Its twenty-two chapters are written by some thirty authors, who are leading experts in their particular subject. The book begins with an overview of the cyanobacteria - or blue-green algae, for those who are not specialists - then looks at their diversity in the geological record and goes on to describe their ecology in present environments where they play important roles. Why is one of the key groups of organisms in the Precambrian still one of the most important groups of phototrophs today? The importance of ecological information for rational management and exploitation of these organisms for commercial and other practical purposes is also assessed. Accounts are provided of nuisances as well as the ecology of the commercially successful Spirulina and the role of cyanobacteria in ecosystem recovery from oil pollution. Many chapters include aspects of physiology, biochemistry, geochemistry and molecular biology where these help general understanding of the subject. In addition there are three chapters dealing specifically with molecular ecology. Thirty-two pages of colour photos incorporate about seventy views and light micrographs. These features make the book valuable to a wide readership, including biologists, microbiologists, geologists, water managers and environmental consultants. The book complements the highly successful The Molecular Biology of Cyanobacteria already published by Kluwer.
Conference Paper
This paper examines the impact of food and energy production on the global N cycle by contrasting N flows in the late-19(th) century with those of the late-20(th) century. We have a good understanding of the amounts of reactive N created by humans, and the primary points of loss to the environment. However, we have a poor understanding of nitrogen's rate of accumulation in environmental reservoirs, which is problematic because of the cascading effects of accumulated N in the environment. The substantial regional variability in reactive nitrogen creation, its degree of distribution, and the likelihood of increased rates of reactive-N formation (especially in Asia) in the future creates a situation that calls for the development of a Total Reactive Nitrogen Approach that will optimize food and energy production and protect environmental systems.
Article
The marine environment, which includes estuarine, coastal and open ocean waters, is a phylogenetically rich repository of planktonic cyanobacteria. All major cyanobacterial groups are represented in the marine plankton, yet specific environmental constraints strongly select for certain groups to dominate in geographically and climatically distinct regions of the world's oceans. In this chapter, physical, chemical and biotic properties of estuarine, coastal and open ocean habitats are examined with respect to their controls on the diversity, abundance and distributions of marine planktonic cyanobacteria. The focus is on the filamentous and colonial cyanobacteria that periodically accumulate as dense blooms that may discolor oceanic and coastal waters. Blooms are of considerable biogeochemical and ecological significance, because they represent large concentrations of phytoplankton biomass that impact carbon, nutrient (N, P, Fe and micronutrients), and oxygen cycling. The smaller coccoid picoplanktonic forms are an additionally important biomass fraction addressed elsewhere (see Chap. 20 by Scanlan). Marine planktonic cyanobacteria employ a suite of morphological, physiological and ecological adaptations and strategies aimed at optimizing growth and reproduction in response to environmental constraints, including nutrient depletion (oligotrophy), variable degrees of turbulence, sub-optimal light and temperature conditions that characterize much of the world's oceans. These include N2 fixation, nutrient sequestration and storage, buoyancy regulation, consortial and symbiotic associations, and coloniality. Specific planktonic taxa are able to exploit human and naturally-(climatic) induced environmental perturbations and changes, such as nutrient-enrichment, rising temperatures, increased tropical cyclone activity, altered rainfall patterns and droughts. Some cyanobacterial bloom taxa are considered harmful (CyanoHABs) because they can negatively affect water quality and habitat condition by producing toxins, exacerbating hypoxia, and altering food webs. Potential nutrient and other management strategies aimed at controlling CyanoHAB outbreaks and dominance are addressed. The extent and limits of biotic evolution in this ancient group of metabolically-diverse phototrophs has strongly affected the geochemical and biotic changes characterizing the evolution of the Earth's oceans and biosphere. © 2012 Springer Science+Business Media B.V. All rights reserved.