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Mitigating the global expansion of harmful cyanobacterial blooms: Moving targets in a human- and climatically-altered world

Authors:
Mitigating the global expansion of harmful cyanobacterial blooms: Moving targets in a human-
and climatically-altered world
Hans W. Paerl
1*
, Malcolm A. Barnard
1
1
Institute of Marine Sciences, University of North Carolina at Chapel Hill, 3431 Arendell St,
Morehead City, NC, USA, *Corresponding Author
Emails:
HWP: hans_paerl@unc.edu
MAB: malcolm.barnard@unc.edu
© 2020 published by Elsevier. This manuscript is made available under the Elsevier user license
https://www.elsevier.com/open-access/userlicense/1.0/
Version of Record: https://www.sciencedirect.com/science/article/pii/S1568988320301244
Manuscript_3e1c6796ba6dc9c71ced439be7d00a4f
1
Abstract 1
Cyanobacterial harmful algal blooms (CyanoHABs) are a major threat to human and environmental 2
health. As global proliferation of CyanoHABs continues to increase in prevalence, intensity, and 3
toxicity, it is important to identify and integrate the underlying causes and controls of blooms in 4
order to develop effective short- and long-term mitigation strategies. Clearly, nutrient input 5
reductions should receive high priority. Legacy effects of multi-decadal anthropogenic eutrophication 6
have altered limnetic systems such that there has been a shift from exclusive phosphorus (P) 7
limitation to nitrogen (N) limitation and N and P co-limitation. Additionally, climate change is 8
driving CyanoHAB proliferation through increasing global temperatures and altered precipitation 9
patterns, including more extreme rainfall events and protracted droughts. These scenarios have led to 10
the “perfect storm scenario”; increases in pulsed nutrient loading events, followed by persistent low-11
flow, long water residence times, favoring bloom formation and proliferation. To meet the 12
CyanoHAB mitigation challenge, we must: (1) Formulate watershed and airshed-specific N and P 13
input reductions on a sliding scale to meet anthropogenic and climatic forcings. (2) Develop 14
CyanoHAB management strategies that incorporate current and anticipated climatic changes and 15
extremes. (3) Make nutrient management strategies compatible with other physical-chemical-16
biological mitigation approaches, such as altering freshwater flow and flushing, dredging, chemical 17
applications, introduction of selective grazers, etc. (4) Target CyanoHAB toxin production and 18
developing management approaches to reduce toxin production. (5) Develop broadly applicable long-19
term strategies that incorporate the above recommendations. 20
21
Keywords: CyanoHABs; N and P Colimitation; Nutrient Legacies; Climate Change; Mitigation 22
Strategies 23
24
2
1. Introduction 25
Global expansion of harmful cyanobacterial blooms (CyanoHABs), is a major threat to safety and 26
sustainability of water supplies for human consumption, agriculture (irrigation), inland fisheries 27
resources, as well as recreational and aesthetic values of impacted waters (Burford et al., 2020; Paerl 28
et al., 2019a, b). Nutrient over-enrichment has been strongly linked to CyanoHAB expansion in 29
aquatic ecosystems (Paerl 1988). This link has a long history; going back at least to eutrophication 30
that spawned massive blooms during the Roman Empire (Haas et al., 2019). Historically, P over-31
enrichment associated with agricultural, urban and industrial development has been identified as a 32
key factor promoting this expansion (Elser and Bennett, 2011; Likens, 1972; Motew et al., 2017; 33
Schindler, 2012; Smith, 2003). As such, reduction of P inputs to CyanoHAB-impacted waters has 34
generally been prescribed as a key bloom mitigation step (Schindler, 2012). Because there are no 35
gaseous forms of P that can potentially escape aquatic ecosystems, P accumulates in both the water 36
column and sediments, leading to a “P legacy”, supporting persistent internal loading which can 37
sustain eutrophication and blooms (Lewis et al., 2011; Reddy et al., 2011). Lake and reservoir 38
systems can have lengthy water residence (or water age) times, often on the order of months to 39
multiple years. Therefore, even if P inputs are reduced, it will take appreciable time to naturally 40
“wean” these systems of internal P supplies (Havens, 1997; Paerl et al., 2016a, b). 41
The other major nutrient element controlling eutrophication, nitrogen (N), while also undergoing 42
excessive anthropogenic enrichment, has gaseous forms (e.g. N
2
, N
2
O, NO, NH
3
), that can readily 43
exchange with the atmosphere. Thus, even though anthropogenic N loading has increased at alarming 44
rates (Erisman et al., 2013; Galloway et al., 2002) and has been shown to be directly implicated in 45
both marine and freshwater eutrophication (Boesch et al., 2001; Conley et al., 2009; Elser et al., 46
2007; Lewis et al., 2011; Nixon, 1995; Ryther and Dunstan, 1971; Wurtsbaugh et al., 2019), there is 47
an “escape route” via gaseous transformation processes. Furthermore, natural inputs of “new” N via 48
3
N
2
fixation are generally exceeded by losses due to in-system denitrification, especially in bloom-49
prone eutrophic systems (Paerl et al., 2016b; Scott et al., 2019). As a result, chronic N limitation is 50
perpetuated, and external N inputs play a key role in maintaining eutrophic, bloom-prone conditions 51
(Paerl et al., 2016b). Furthermore, recent studies have stressed the need to reduce N inputs into 52
CyanoHAB-plagued systems due to the ties between N inputs, CyanoHAB growth and toxicity 53
(Gobler et al., 2016; Harke et al., 2016; Shatwell and Köhler, 2019). Clearly, there is good reason to 54
constrain external loads of both N and P, and impose more nutrient-limited conditions in order to 55
help mitigate the CyanoHAB problem (Chaffin and Bridgeman, 2014; Müller and Mitrovic, 2015; 56
Zohary et al., 2005). 57
Therefore, while P input reductions should be part of any long-term eutrophication and 58
CyanoHAB control strategy, in order to speed up the “de-eutrophication” or “oligotrophication” 59
process, parallel N input reductions are urgently needed, especially in light of global agricultural, 60
urban and industrial expansion (Paerl et al., 2019 a). 61
62
2. Legacy Effects of Nutrients in Freshwater Ecosystems 63
The term legacy effect entered the scientific literature in the late 1980s and early 1990s (Corbet, 64
1985; Molina and Amaranthus, 1991). Legacy effects are defined as the impacts that one generation 65
leaves on the environment for future generations to inherit (Button et al., 1999). In ecological terms, 66
legacy effects can be considered to be ecological inheritance (Cuddington, 2011). In freshwater 67
ecosystems, nutrient legacy effects add to the issues related to anthropogenic eutrophication (Duff et 68
al., 2009). A large portion of the nutrient legacy is driven by land use and land cover changes, which 69
have led to nutrient-enriched urban and agricultural runoff (Bain et al., 2012; Martin et al., 2011). 70
Since the rapid increases in chemical fertilizer use after WWII, nutrient loading has accelerated 71
dramatically (Haygarth et al., 2014). As mentioned earlier, P can mainly leave aquatic systems by 72
flushing or ending up in the sediments. Approximately 20−30% of P applied to agricultural land is
73
4
exported directly out of the watershed as crop and animal production. The remaining 70−80% of the 74
applied P ends up as stores in soils, river sediments, groundwater, wetlands, riparian floodplains, 75
lakes, and estuaries (Jarvie et al., 2013; Sharpley et al., 2013). Even though N can leave the aquatic 76
systems as gases, some N also end up leaving a legacy on water bodies. Anthropogenic loading of N 77
into agricultural soils can leach into groundwater, leading to an N legacy in aquifers (Puckett et al., 78
2011). A substantial fraction of accumulated CyanoHAB biomass is decomposed in the water 79
column and surface sediments, fueling hypoxia (< 2.0 mg O
2
L
-1
) and anoxia (< 0.5 mg O
2
L
-1
) 80
(Buzzelli et al., 2002; Paerl, 2014). The biomass fraction that is not immediately decomposed ends 81
up in the sediments as legacy organic carbon, organic N, and organic P. Legacy nutrients provide for 82
a positive feedback loop supporting CyanoHAB growth (Figure 1), and it is a key reason why 83
reversing the harmful effects of eutrophication can take a substantial amount of time, especially in 84
large, long water residence time aquatic ecosystems (Paerl et al., 2019b). 85
86
3. Climate Change Effects on Nutrient Loading in Freshwater Ecosystems 87
While nutrient input reductions represent the “bottom line” in mitigating eutrophication and 88
CyanoHAB expansion, there are additional, interacting drivers modulating this process, the most 89
prominent and challenging being climate change (Paerl and Paul, 2012). Global warming, changes in 90
precipitation patterns and amounts and altered wind speeds are strong modulators of eutrophication 91
and CyanoHAB expansion (Deng et al., 2018; Paerl et al., 2016a; Paerl and Huisman, 2009, 2008; 92
Weber et al., 2020). Both of these symptoms of climate change are increasing in frequency and 93
geographic distribution (Burford et al., 2020; Sinha et al., 2017; Trenberth, 2008; Wuebbles et al., 94
2013). Increasing temperatures, stronger vertical stratification, and salinization are also associated 95
with climate change and linked to CyanoHAB magnitudes, frequency, distribution and duration 96
(Chapra et al., 2017; Moore et al., 2008; Paerl, 2017; Paerl et al., 2011; Paerl and Huisman, 2009, 97
5
2008). As pointed out in Paerl et al., (2016a), the “perfect storm” scenario for CyanoHAB 98
development and proliferation is excessive episodic rainfall events, followed by droughts, which can 99
promote large nutrient input pulses followed by lengthy residence times, enabling blooms to develop 100
and proliferate. Increased temperatures and nutrient loading can also enhance CyanoHAB toxicity 101
(Botana, 2016; Gehringer and Wannicke, 2014; Lehman et al., 2013; Moe et al., 2013). Furthermore, 102
it is likely that these nutrient reduction thresholds will change with changing climatic conditions, 103
human watershed and airshed activities, as populations continue to change (Erisman et al., 2013; 104
Galloway et al., 2002; Moss et al., 2008; Peierls et al., 1991). Wildfires brought on by climate change 105
can also lead to nutrient loading due to increased mobility of sediment (Emelko et al., 2016), 106
especially when followed by extensive rainfall and flooding as has been the case in California and 107
most recently in Eastern and Southern Australia (Malmsheimer et al., 2008; Sharples et al., 2016). In 108
addition to enhancing P inputs associated with sediment mobilization, deforestation also leads to N 109
loading, as seen in N cycle shifts the Laurentian Great Lakes (Guiry et al., 2020). Therefore, changes 110
in these climatic drivers will need to be incorporated into the development of nutrient input 111
reductions that will effectively maintain bloom potentials below specific nutrient loading thresholds 112
for individual water bodies. Warming and nutrient loading and temperature synergistically increase 113
the intensity and recurrence of CyanoHABs, which amplify the feedback loop promoting CyanoHAB 114
growth (Figure 1). 115
Anthropogenic influences on the atmosphere are also modulating CyanoHABs. Increasing 116
atmospheric pCO
2
can enhance phytoplankton blooms, including CyanoHABs (Verspagen et al., 117
2014). The augmented pCO
2
will also favor CyanoHAB growth due to rapid adaptation to higher 118
pCO
2
environments as seen in microcosm and chemostat experiments (Sandrini et al., 2016; Shi et 119
al., 2017; Ji et al., 2020). While the effects of increased pCO
2
appear to promote CyanoHABs, much 120
less is known about the in situ mechanisms compared to the effects of temperature (Verspagen et al., 121
2014; Ji et al., 2020). In addition to atmospheric carbon emissions, N and P emissions also impact 122
6
CyanoHAB proliferation. Atmospheric deposition has been shown to be significant source of both N 123
and P into aquatic systems. For example, Paerl et al., (2002) estimated that from 20 to >35% of N 124
inputs to N-limited US Atlantic estuarine and coastal waters was attributed to atmospheric N 125
deposition, while 63% of total N and 42% of total P loading in Cultus Lake near Vancouver, BC, 126
Canada, come from atmospheric deposition (Putt et al., 2019). Atmospheric deposition also indirectly 127
impacts coastal systems, as an average of 64% of riverine N export to coastal ocean systems is 128
derived from NO
x
and NH
x
deposition (Church and Sickle, 1999; Jaworski et al., 1997). Groundwater 129
inputs of N and P, much of it due to human pollution, provide an additional source of nutrients 130
promoting eutrophication along the freshwater to marine continuum (Paerl, 1997). The combined 131
effect of increased anthropogenic surface, subsurface and atmospheric nutrient loading, in addition to 132
promoting eutrophication, has driven receiving waters into N and P co-limitation and N-limitation 133
(Chaffin et al., 2014; Dodds and Smith, 2016; Elser et al., 2007). 134
135
4. Management Recommendations 136
When reducing external N&P loading, both point-source and nonpoint-source nutrient inputs 137
need to be addressed. Point source pollution is the easiest target for N and P reduction, as this source 138
can be reduced by targeting readily identified and well-defined origins, such as effluents from 139
wastewater treatment plants and industrial discharge points (Hamilton et al., 2016; Wu et al., 2006). 140
Reduction in point source pollution generally involves diversion of sewage from waterbodies and 141
reduction in P and N concentrations in the wastewater discharge (Sedlak, 1991). N removal from 142
wastewater generally makes use of coupled nitrification–denitrification (US EPA, 2013). P removal 143
occurs either through burial or flushing of P bound in biomass out of the system (Downing, 1997). 144
Buried P can be removed by dredging (Reddy et al., 2007), although a short term P spike often 145
results from dredging (Smith et al., 2006). While P-based detergent bans have been successful at 146
7
reducing blooms (Dolan and McGunagle, 2005), there are cases where P from detergents continues to 147
be an important component of P in surface waters while also imposing a major burden on wastewater 148
treatment processes (Hamilton et al., 2016; Van Drecht et al., 2009). Greater attention needs to be 149
focused on nonpoint sources of nutrients, which in many watersheds is the largest source of nutrient 150
loading and is often dominated by agriculture (Hamilton et al., 2016). Furthermore, nonpoint-source 151
pollution continues to increase as a relative proportion of total loading as more advanced treatment of 152
point source pollution is implemented (Hamilton et al., 2016). Removing N and P from stormwater 153
runoff can be achieved by using combined wetlands and infiltration ponds to naturally filter N and P 154
(Marsalek and Schreier, 2009; Zheng et al., 2006). Retaining fertilizer-based N and P in agricultural 155
soils should receive high priority (Hamilton et al., 2016). Maintaining N and P in soils at levels close 156
to or below agronomic optima is critical and represents one of the simplest and most cost-effective 157
methods to reduce eutrophication in receiving waters (Drewry et al., 2006; Rasouli et al., 2014). 158
Where feasible, fertilizer should be directly injected into the soil to minimize nutrient-rich surface 159
runoff (Seo et al., 2005). 160
Another method of removing nutrients from non-point sources is through in situ biological 161
filtration, using non-harmful algal “scrubber” and “raceway” devices (Adey et al., 2013; Barnard et 162
al., 2017; Mulbry et al., 2010, 2008). Adding denitrifying bacteria can greatly speed up N removal 163
(Chen et al., 2017). Vegetated buffers are also a useful tool for remediating nonpoint source 164
pollution; trees, shrubs and grasses in the vegetated buffer have been shown to remove more than 165
85% of pollutants (Zhang et al., 2010), including 85% of N and 84% of P (Polyakov et al., 2005). 166
However, the biomass from buffers needs to be periodically harvested and exported in order to have 167
net nutrient removal effect, unless processes such as denitrification are additionally enhanced by this 168
approach (Hoffmann et al., 2009). Additionally, natural and constructed wetlands are very effective, 169
low cost solutions for removal of nonpoint source nutrients from aquatic systems (O’Geen et al., 170
8
2010; Ribaudo et al., 2001), with removal of over 80% of N loading and over 50% of P loading 171
(Braskerud, 2002a, 2002b; Kao and Wu, 2001). 172
There is a significant association between cyanobacterial blooms and land use types (i.e., 173
industrial, commercial, and transport areas) (Arthington, 1996; Soranno et al., 1996). These results 174
are relevant to landscape planning for mitigating future impacts of climate change on the drainage 175
network, surface runoff, nutrient loads and, ultimately, on the development of toxigenic 176
cyanobacteria (Hamilton et al., 2016). A better knowledge of the relationships between land use type 177
and discharge is essential to foresee the effects of climate change on drainage basins and therefore to 178
evaluate potential triggers of CyanoHABs (Jimenez Cisneros et al., 2014). 179
Higher amounts of freshwater runoff can enhance vertical density stratification (reduced vertical 180
mixing) in waters having appreciable salinity, including estuarine and coastal waters as well as saline 181
lakes and rivers; by allowing relatively light freshwater lenses to establish themselves on top of 182
heavier (denser) saltwater. The resultant enhanced vertical stratification will favor CyanoHABs 183
capable of rapid vertical migration to position themselves at physically-chemically favorable depths 184
in both freshwater and marine systems (Paerl, 2014; Paerl and Huisman, 2009) by rapidly altering 185
their buoyancy in response to varying light, temperature and nutrient regimes (Walsby et al., 1997). 186
The large biomass and long survival time of CyanoHABs in sediments can help explain the 187
delayed recovery of affected lakes after reduction of external nutrient loads (Brunberg and Boström, 188
1992; Paerl et al., 2016a). Sediment removal involves expensive dredging and disturbance of lake 189
bottoms, which can release additional nutrients (and potentially toxic substances) and adversely 190
affect benthic flora and fauna. However, CyanoHABs were eradicated successfully with this 191
approach in Lake Trummen, Sweden (1 km
2
, mean depth 1.6 m), which experienced CyanoHABs 192
and water quality degradation from domestic sewage and industrial nutrient inputs during the mid-193
1900s (Cronberg, 1982; Peterson, 1982). Suction dredging the upper half-meter of sediments over 194
9
two years led to significant decreases in nutrient concentrations and CyanoHABs (Cronberg, 1982; 195
Peterson, 1982). Lake Trummen’s rapid CyanoHAB eradication is attributed to its small size and the 196
ability to simultaneously reduce external nutrient loads effectively from its small size (13 km
2
) 197
(Cronberg, 1982; Peterson, 1982). Dredging is not a feasible solution for reducing internal P loading 198
in large lakes, where P-rich sediments are distributed over hundreds or thousands of square 199
kilometers and are highly mobile (James and Pollman, 2011). 200
CyanoHABs can be treated with chemical and/or biological agents to limnetic systems. Chemical 201
treatments, including precipitation and immobilization of phosphorus in bottom sediments (Phoslock, 202
alum, etc.), application of algaecides (Cu compounds, hydrogen
peroxide, permanganate, etc.), as 203
well as biological controls, such as the introduction of invertebrate and fish grazers, lytic bacteria, 204
and viruses, may temporarily halt the advance of CyanoHABs (Matthijs et al., 2012; Paerl et al., 205
2015; Pan et al., 2006; Robb et al., 2003). However, there are unintended negative impacts on flora 206
and fauna of the limnetic systems that make these chemical treatments potentially detrimental to 207
these systems (Bishop et al., 2018; Escobar-Lux et al., 2019; Paerl et al., 2015). Addition of selective 208
grazers is another option, but successful control of CyanoHABs by grazers is unlikely except in 209
specific cases (Paerl et al., 2001). This is due to cyanobacteria being generally considered to be 210
relatively low preference foods for marine and freshwater herbivores because of chemical and 211
structural defenses and poor nutritional quality (Cruz-Rivera and Villareal, 2006; DeMott and 212
Moxter, 1991; Paerl et al., 2001; Paerl and Paul, 2012). The addition of the grazers can also have 213
negative effects on the food webs through trophic cascades (Jeppesen et al., 2007; Wright and 214
Shapiro, 1984). Given the lack of feasibility, unpredictable and unintended effects of chemical and 215
biological additions, the most prudent and defensible approach is to prioritize nutrient input 216
reductions; however, if nutrient reduction is not enough to reduce the impacts of the blooms, then 217
reassessment of nutrient reduction thresholds as well as the use of any of the above mitigation 218
methods should be considered to manage the CyanoHABs. 219
10
Remote sensing technology can be useful for tracking and evaluating management of blooms as a 220
means of linking nutrient sources to bloom dynamics over varying temporal and spatial scales 221
(Dorigo et al., 2007; Field et al., 1995; Mishra et al., 2019). Using remote sensor networks, satellite 222
imagery, and machine learning, the extent and drivers of CyanoHABs can be remotely sensed and 223
analyzed (Davis et al., 2019; Mishra et al., 2018, 2019; Zhang et al., 2016). Satellite-based imagery 224
paired with Raspberry-Pi-based remote sensors (CyanoSense), cellular-phone-based application 225
CyanoTracker, and social networking services such as Twitter can document the progression and 226
proliferation of blooms (Boddula et al., 2017; Mishra et al., 2018, 2019; Page et al., 2018; Scott et al., 227
2016; Stumpf et al., 2016). While satellite imagery can measure biomass in CyanoHABs using the 228
different spectral properties of chlorophyll and phycocyanin (Binding et al., 2019), it cannot 229
accurately measure cyanotoxin production as CyanoHAB cellular toxin content can vary even on 230
short time scales and can persist extracellularly after bloom biomass is dissipated (Davis et al., 2019). 231
Therefore, remote sensing should be paired with long-term monitoring. On-lake long-term 232
monitoring of water quality parameters is also critical for protecting human exposure to cyanotoxins 233
during blooms (Davis et al., 2019). Management recommendations are outlined in Figure 2. 234
Anthropogenic forcing continues to alter natural systems and the climate, with major 235
ramifications for nutrient loading, hydrologic changes (e.g., more intense and larger rainfall and 236
flooding events), warming and changes in wind speed - all of which will alter the rates of 237
eutrophication and nutrient-bloom threshold relationships. This calls for the formulation of adaptive 238
nutrient management strategies aimed at maintaining bloom potentials and proliferation below 239
critical nutrient-bloom thresholds. Given the current trajectory of climate change (warming, more 240
extreme wet/dry cycles, reduced wind speed in many locations), it is likely that nutrient loading 241
threshold levels above which blooms will occur, will be lowered, because CyanoHABs will grow 242
more efficiently at elevated temperatures and persist longer under extreme wet/dry cycles (Paerl et 243
11
al., 2016a). Furthermore, with more extensive wet/dry cycles, both external and internal nutrient 244
cycling will be altered, and this will likely benefit CyanoHABs, which can affect internal cycling by 245
lasting longer during the growth season and can promote positive feedbacks on sediment-water 246
column nutrient cycling to maintain blooms (Fig. 1). This is especially true if CyanoHABs are not 247
effectively consumed by grazers and ultimately finfish or shellfish, which can be exported from the 248
system. More likely, CyanoHAB biomass will enter the detrital-microbial loop component of nutrient 249
cycling, enhancing microbial decomposition and recycling of nutrients more effectively during a 250
single growth season. Overall, this means that current nutrient loading targets aimed at controlling 251
CyanoHABs will need to be set at lower levels than currently prescribed for many regions. With 252
legacy nutrients and climate change leading to positive feedback loops of cyanoHAB proliferation, 253
we need to focus on watershed and airshed nutrient reductions that can help reduce and ultimately 254
break the loops. Lastly, we can complement these efforts with (where feasible and effective) 255
biological and chemical treatments, remote sensing technology, and routine monitoring to help 256
manage CyanoHABs into the future. 257
258
Acknowledgments 259
This work was supported by the USA National Science Foundation (1803697, 1831096), the 260
National Institutes of Health (1P01ES028939-01), a Grant-in-Aid of Research from Sigma Xi, The 261
Scientific Research Society (G201903158412545), and the NOAA/North Carolina Sea Grant 262
Program R/MER-43, R/MER-47. We would like to thank two anonymous reviewers for their 263
constructive feedback on the manuscript. 264
265
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Figure 1. Conceptual diagram, showing the feedback loops of climatic effects and nutrients on 681
CyanoHAB biomass. a) Climate change is causing more intense wet/dry cycles, widespread 682
wildfires, and warming, leading to an increase in CyanoHAB biomass. b) Increased CyanoHAB 683
biomass is involved in a positive feedback loop with legacy nutrients and regenerated nutrients 684
derived from the microbial loop. c) These feedback loops combined with climatic effects constitute a 685
key challenge to mitigating CyanoHABs. 686
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Figure 2. Conceptual diagram, illustrating multiple, interacting controls in CyanoHAB management. 688
Climatic influences have led to the need to reduce nutrient loading below previous reduction 689
standards, putting additional pressure on reducing nutrient inputs from (a) point source pollution and 690
(b) non-point source pollution, (c) regenerated nutrients, and (d) legacy nutrients though various 691
mechanical, chemical, and biological means. (e) Short-term (several months) treatment, chemical and 692
biological approaches used. (f) Appropriate monitoring is essential for assessing the CyanoHAB 693
scales and the efficacy of management approaches. 694
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... Toxigenic (i.e., possessing MC-producing genes) and non-toxigenic Microcystis genotypes are often mixed without full segregation in blooms (Pearson et al., 2016), which has occasionally caused severe poisoning episodes in humans, domestic animals and wildlife all over the world (Svirčev et al., 2019). Considering the above environmental factors favoring the development of cyanoHABs, several prevention or mitigation strategies have been proposed such as: artificial mixing of the water column, phosphorus precipitation, sediment dredging, hydrogen peroxidation, chemical restoration or ultrasounds (Paerl and Barnard, 2020;Sinha et al., 2018;Visser et al., 2016). However, these actions often require time, continuous information on climatic and physicochemical data, large financial investment for operational and initial capital costs, or simply do not provide the expected results (Lürling et al., 2015). ...
... Over the last decade, biological control is receiving increasing attention as a nature-based solution to cope with cyanoHABs. The introduction of zooplankton and fish grazers, aquatic plants, natural substances extracted from plants, and algicidal microorganisms (i.e., fungus, bacteria and viruses) are some potential strategies to effectively control the advance of cyanobacterial proliferation (Paerl and Barnard, 2020;Sun et al., 2018;Zerrifi et al., 2021). Bacteria with algicidal activity are of particular interest because they are natural antagonists of blooming cyanobacteria, with a major role in bloom decay . ...
Article
Cyanobacterial harmful algal blooms (cyanoHABs) are a global problem with serious consequences for public health and many sectors of the economy. The use of algicidal bacteria as natural antagonists to control bloom- forming cyanobacteria is a topic of growing interest. However, there are still unresolved questions that need to be addressed to better understand their mode of action and to implement effective mitigation strategies. In this study, thirteen bacterial strains isolated from both scums and concentrated bloom samples exhibited algicidal activity on three Microcystis aeruginosa strains with different characteristics: the axenic microcystin (MC)-pro- ducing strain M. aeruginosa PCC7820 (MaPCC7820), and two environmental (non-axenic) M. aeruginosa strains isolated from two different water bodies in Poland, one MC-producer (MaSU) and another non-MC-producer (MaPN). The bacterial strain SU7S0818 exerted the highest average algicidal effect on the three cyanobacte- rial strains. This strain was identified as Morganella morganii (99.51% similarity) by the 16S rRNA gene analyses; hence, this is the first study that demonstrates the algicidal properties of these ubiquitous bacteria. Microscopic cell counting and qPCR analyses showed that M. morganii SU7S0818 removed 91%, 96%, and 98.5% of MaPCC7820, MaSU and MaPN cells after 6 days of co-culture, respectively. Interestingly, the ultra-high-performance liquid chromatography-tandem mass spectrometer (UHPLC-MS/MS) analyses showed that this bacterium was involved on the release of several substances with algicidal potential. It was remarkable how the profile of some compounds evolved over time, as in the case of cadaverine, tyramine, cyclo[Pro-Gly] and cyclo [Pro-Val]. These dynamic changes could be attributed to the action of M. morganii SU7S0818 and the presence of associated bacteria with environmental cyanobacterial strains. Therefore, this study sheds light on how algicidal bacteria may adapt their action on cyanobacterial cells by releasing a combination of compounds, which is a crucial insight to exploit them as effective biological tools in the control of cyanoHABs.
... Despite this, management of cHABs in freshwater systems remains largely based upon the characterisation of ideal conditions for growth, proliferation, and toxin production of cyanobacteria at the species level, often focusing primarily on temperature and nutrient concentration and bioavailability (Ho & Michalak, 2020;Paerl & Barnard, 2020;Przytulska et al., 2017). Recent molecular work (e.g. ...
Article
Abstract 1. Freshwater cyanobacterial harmful algae blooms (cHABs) are a major threat to human and environmental health and are increasing globally in frequency and severity. To manage this threat in a timely manner, science must focus on increasing our ability to predict the growth and toxigenicity of specific taxa of cyanobacteria. 2. Recent molecular research has revealed striking genomic and metabolic diversity among the many morphologically indistinguishable sub-species and strains of cyanobacteria. Assemblage-level molecular metabolic capability surveys promise to improve our ability to predict cyanobacterial responses to environmental forcing, but many of these cutting-edge techniques are not widely available or cost-effective enough to be employed in routine monitoring programmes to support management decisions. Taxonomic ambiguity, cryptic functional specialisation, incongruence between genomic capability and phylogeny, and genomic flexibility impose severe challenges to our ability to ascribe autecological attributes at a level of taxonomic resolution that is attainable under current management strategies (i.e. Linnaean species). This lack of knowledge prohibits reliable predictions of species' responses to environmental stressors. 3. Cyanobacterial species comprise consortia of metabolically diverse, morphologically indistinct strains that span a range of ecological specialisation. Under current, broadly applied taxonomic concepts, these species functionally embody a generalist ecological strategy—persisting and/or proliferating where other specialised competitors are negatively impacted. 4. We postulate that within current management frameworks, characterising of cyanobacterial species as competing generalists, as well as considering abundance trajectories of well-characterised, non-cyanobacterial specialist phytoplankton will generate more scalable, mechanistic, and management-relevant insight into increasing cHAB frequency and severity in suitable time frames. 5. Here we recommend that cHAB management considers the competitive framework of phytoplankton communities, including cyanobacteria, wherein diverse environmental changes lead to deterministic responses by readily identifiable, documented specialist taxa. Characterising these changes in community structure will quantify the relative importance of altered stressors and resource availability that can be exploited by metabolically flexible cyanobacteria.
... They were primarily referred to the following filamentous genera: Anabaena, Aphanizomenon, Blennothrix, Chrysosporum, Cuspidothrix, Cylindrospermum, Dolichospermum, Kamptonema, Lyngbya, Microcoleus, Microseira, Moorea, Nostoc, Oscillatoria, Planktothrix, Phormidium, Raphidiopsis (Syn. Cylindrospermopsis), Sphaerospermopsis and Tychonema [1-11], but two coccal genera, colonial Microcystis and Woronichinia, were also proved to be ATX producers [1, 12,13]. The ability of cyanoprokaryotes to produce ATX is generic-and species-dependent, but one and the same species may comprise strains that are atoxic, while others can produce toxic metabolites [1,3]. ...
Article
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The paper presents the first proof of planktonic cyanoprokaryote genus Cuspidothrix as an anatoxin A (ATX) producer in Bulgarian wetlands. The results from polymerase chain reaction (PCR) obtained from two summer sampling campaigns in 26 selected lakes and reservoirs demonstrated presence of the anaC gene, responsible for ATX production in 21 strains of the genus. They were found in three waterbodies sampled in 2018 (coastal lake Vaya, coastal reservoir Poroy, inland reservoir Sinyata Reka) and in four waterbodies sampled in 2019 (inland reservoirs Duvanli, Koprinka, Plachidol 2, Sinyata Reka). The detected genetic diversity generally corresponds to the observations conducted by conventional light microscopy, by which we distinguished three species of Cuspidothrix (Cuspidothrix issatschenkoi, Cuspidothrix elenkinii and Cuspidothrix tropicalis, the latter considered alien in the country). Eleven strains showed high similarity to two sequences of C. issatschenkoi available from the National Centre for Biotechnology Information (NCBI). Ten other strains assembled in a group, which—in lack of available from NCBI genetic sequences—were presumed related to C. tropicalis and C. elenkinii after comparison with the results from light microscopy. Cuspidothrix strains found in Bulgarian waterbodies showed high genetic similarity to those isolated and sequenced from Asia (Japan, China) and Northern Europe (Norway, Finland).
... The growth of T&O producing microbes is strongly affected by environmental conditions such as nutrient concentration, light availability, water temperature, and hydrodynamics (Davies et al., 2004;Su et al., 2019;Zhang et al., 2019). These risk factors have been extensively reviewed, with a focus on toxin production by algae (Burford et al., 2020;Harke et al., 2016;Huisman et al., 2018;Paerl and Barnard, 2020;. However, the biosynthesis pathways and microbial ecology of T&O production differ to toxin production, and T&O risk factors are not well understood (Fig. 3). ...
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Biogenic taste and odour (T&O) have become a global concern for water utilities, due to the increasing frequency of algal blooms and other microbial events arising from the combined effects of climate change and eutrophication. Microbially-produced T&O compounds impact source waters, drinking water treatment plants, and drinking water distribution systems. It is important to manage across the entire biogenic T&O pathway to identify key risk factors and devise strategies that will safeguard the quality of drinking water in a changing world, since the presence of T&O impacts consumer confidence in drinking water safety. This study provides a critical review of current knowledge on T&O-causing microbes and compounds for proactive management, including the identification of abiotic risk factors in source waters, a discussion on the effectiveness of existing T&O barriers in drinking water treatment plants, an analysis of risk factors for biofilm growth in water distribution systems, and an assessment of the impacts of T&O on consumers. The fate of biogenic T&O in drinking water systems is tracked from microbial production pathways, through the release of intracellular T&O by cell lysis, to the treatment of microbial cells and dissolved T&O. Based on current knowledge, five impactful research and management directions across the T&O pathway are recommended.
... Identifying and defining their interactions is critical for the understanding of how these complex microbial communities respond to and recover from disturbances, such as algal blooms (Woodhouse et al., 2016). Global expansion of harmful cyanobacterial blooms in inland waters, which arises from human activities and global warming, is one of the most profound disturbances to aquatic microorganisms at present (Huisman et al., 2018;Paerl and Barnard, 2020). ...
Article
Unraveling how microbial co-occurrences respond to cyanobacterial blooms is central to our understanding of the stability of aquatic ecosystems. Here, we examined the effects of a Microcystis bloom on the inter-domain eukaryotic and two size-fractionated bacterial networks in a subtropical reservoir. Eukaryotes, especially pro-tists, had a central role in microbial networks, followed by particle-attached (PA) bacteria and free-living (FL) bacteria. Eukaryotes had more negative correlations with PA bacteria than with FL bacteria. The environmental changes related to the Microcystis bloom (i.e., water temperature, pH, chlorophyll a, total carbon, total organic carbon and nitrite nitrogen) strongly affected eukaryotes and PA bacteria network as reflected by the dynamics of community composition in major modules. Importantly, the network complexity and stability significantly increased in the post-bloom periods, and eukaryotes (especially protists) enhanced the stability of the microbial network. Compared to keystone FL bacteria, eukaryotic and PA bacterial hubs mainly determined the network structure and key functional potentials (i.e., nitrogen cycling, carbon fixation and carbon degradation). Thus, some keystone eukaryotes and PA bacteria might be used as indicators of the structure and function stability of microbial communities in reservoir ecosystems. Our study highlights the importance of considering microbial cross-kingdom and multiple size-fractionation correlations in evaluating the effects of environmental disturbances on microbial networks.
... Phytoplankton blooms in global inland waters have demonstrated a noticeably increasing trend, which is likely attributable to eutrophication, global warming and increasing hydrologic variability (Ho et al., 2019;Huisman et al., 2018;Shi et al., 2019). The worldwide expansion of phytoplankton blooms has severely threatened water quality, food webs, habitat stability and human health (Paerl and Barnard, 2020;Paerl and Huisman, 2008;Taranu et al., 2012). In particular, phytoplankton blooms can increase turbidity, thereby decreasing light availability and suffocating submerged aquatic vegetation (Bricker et al., 2008;Shi et al., 2014). ...
Article
The worldwide expansion of phytoplankton blooms has severely threatened water quality, food webs, habitat stability and human health. Due to the rapidity of phytoplankton migration and reproduction, high-frequency information on phytoplankton bloom dynamics is crucial for their forecasting, treatment, and management. While several approaches involving satellites, in situ observations and automated underwater monitoring stations have been widely used in the past several decades, they cannot fully provide high-frequency and continuous observations of phytoplankton blooms at low cost and with high accuracy. Thus, we propose a novel ground-based remote sensing system (GRSS) that can monitor real-time chlorophyll a concentrations (Chla) in inland waters with a high frequency. The GRSS mainly consists of three platforms: the spectral measurement platform, the data-processing platform, and the remote access control, display and storage platform. The GRSS is capable of obtaining a remote sensing irradiance ratio (R(λ)) of 400-1000 nm at a high frequency of 20 seconds. Eight different Chla retrieval algorithms were calibrated and validated using a dataset of 481 pairs of GRSS R(λ) and in situ Chla measurements collected from four inland waters. The results showed that random forest regression achieved the best performance in deriving Chla (R² = 0.95, root mean square error = 13.40 μg/L, and mean relative error = 25.7%). The GRSS successfully captured two typical phytoplankton bloom events in August 2021 with rapid changes in Chla from 20 μg/L to 325 μg/L at the minute level, highlighting the critical role that this GRSS can play in the high-frequency monitoring of phytoplankton blooms. Although the algorithm embedded into the GRSS may be limited by the size of the training dataset, the high-frequency, continuous and real-time data acquisition capabilities of the GRSS can effectively compensate for the limitations of traditional observations. The initial application demonstrated that the GRSS can capture rapid changes of phytoplankton blooms in a short time and thus will play a critical role in phytoplankton bloom management. From a broader perspective, this approach can be extended to other carriers, such as aircraft, ships and unmanned aerial vehicles, to achieve the networked monitoring of phytoplankton blooms.
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The cyanobacteria-associated microbiome is constantly reshaped by bloom development. However, the synergistic-antagonistic nature of the relationships between Microcystis and its microbiome still remains unclear. Therefore, temporal changes of bacterioplankton communities and their functional potential through different developing stages of a Microcystis toxigenic bloom were investigated, considering bacterioplankton assemblages as particle-attached (PAB) and free-living (FLB) bacteria. 16S rRNA sequencing revealed that PAB were represented by Proteobacteria and Cyanobacteria, while FLB by Proteobacteria and Actinobacteria. Network and ordination analyses indicated that PAB inter-relationships were more complex—numerous connections between taxa with stronger correlations, than FLB—rather influenced by physico-chemical parameters. PAB in pre-summer was diverse with Proteobacteria containing potential taxa involved in nitrogen-transforming processes. In mid-summer, PAB presented a mix-bloom dominated by Snowella, Aphanizomenon, and Microcystis, which were succeeded by toxigenic Microcystis in post-summer. Both periods were associated to potential taxa with parasitic/predatory lifestyles against cyanobacteria. In post-summer, Sutterellaceae were recognized as poor water quality indicators, and their strong association with Microcystis could have represented an increased threat for that period. Microcystis was a major factor significantly reducing PAB diversity and evenness, suggesting that it negatively influenced bacterioplankton assemblages, probably also altering the overall community functional potential.
Article
Cyanobacterial harmful algal blooms (cyanoHABs) are an ecological concern because of large ecosystem-disrupting blooms and a global public health concern because of the cyanotoxins produced by certain bloom-forming species. Another threat to global public health is the dissemination of antibiotic resistance (AR) in freshwater environmental reservoirs from anthropogenic sources, such as wastewater discharge and urban and agricultural runoff. Cyanobacteria are now hypothesized to play a role in the environmental resistome. A non-systematic literature review of studies using molecular techniques (such as PCR and metagenomic sequencing) was conducted to explore indirect and direct ways cyanobacteria might contribute to environmental AR. Results show cyanobacteria can host antibiotic resistance genes (ARGs) and might promote the spread of ARGs in bacteria due to the significant contribution of mobile genetic elements (MGEs) located in genera such as Microcystis. However, cyanobacteria may promote or inhibit the spread of ARGs in environmental freshwater bacteria due to other factors as well. The purpose of this review is to 1) consider the role of cyanobacteria as AR hosts, since cyanoHABs are historically considered to be a separate problem from AR, and 2) to identify the knowledge gap in understanding cyanobacteria as ARG reservoirs. Cyanobacterial blooms, as well as other biotic (e.g. interactions with protists or cyanophages) and abiotic factors, should be studied further using advanced methods such as shotgun metagenomic and long read sequencing to clarify the extent of their functional ARGs/MGEs and influences on environmental AR.
Article
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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Photosynthetic micro-organisms are equipped with molecular machineries that are designed to transform light into chemical or bioenergy, and help shape and balance the ecosystem of all life forms on earth. Recently, aquatic ecosystems have been disrupted by climate change, which leads to the frequent occurrence of harmful algal blooms (HABs). HABs endanger drinking water resources and harm the fishing and coastal recreation industries. Despite its urgency, mechanistic understanding of how key biophysical and biochemical parameters impact algal growth is largely unexplored. In this article, we developed a microscope-based light gradient generator for studies of photosynthetic micro-organisms under well-defined light intensity gradients. This technology utilized a commercially available microscope, allowed for controlled light exposure and imaging of cells on the same microscope platform, and can be integrated with any micrometer-scale device. Using this technology, we studied the role of light intensity in the growth of photosynthetic micro-organisms. A parallel study was also carried out using a 96-well plate. Our work revealed that the growth rate of the microalgae/cyanobacteria was significantly regulated by the light intensity and followed Monod or van Oorschot kinetic models. The measured half-saturation constants were compared with those obtained in macro-scale devices, and indicated that shading, light spectrum, and temperature may all play important roles in the light sensitivity of photosynthetic micro-organisms. This work highlighted the importance of analytical tools for quantitative understanding of biophysical parameters in the growth of photosynthetic micro-organisms, and knowledge learned will be critical in the design of future technologies for managing algal blooms or optimizing bioenergy production.
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Although phenotypic plasticity is a widespread phenomenon, its implications for species responses to climate change are not well understood. For example, toxic cyanobacteria can form dense surface blooms threatening water quality in many eutrophic lakes, yet a theoretical framework to predict how phenotypic plasticity affects bloom development at elevated p CO 2 is still lacking. We measured phenotypic plasticity of the carbon fixation rates of the common bloom-forming cyanobacterium Microcystis . Our results revealed a 1.8- to 5-fold increase in the maximum CO 2 uptake rate of Microcystis at elevated p CO 2 , which exceeds CO 2 responses reported for other phytoplankton species. The observed plasticity was incorporated into a mathematical model to predict dynamic changes in cyanobacterial abundance. The model was successfully validated by laboratory experiments and predicts that acclimation to high p CO 2 will intensify Microcystis blooms in eutrophic lakes. These results indicate that this harmful cyanobacterium is likely to benefit strongly from rising atmospheric p CO 2 .
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