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Climate Change and the Potential Spreading of Marine Mucilage and Microbial Pathogens in the Mediterranean Sea

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Climate Change and the Potential Spreading of Marine Mucilage and Microbial Pathogens in the Mediterranean Sea

Abstract and Figures

Marine snow (small amorphous aggregates with colloidal properties) is present in all oceans of the world. Surface water warming and the consequent increase of water column stability can favour the coalescence of marine snow into marine mucilage, large marine aggregates representing an ephemeral and extreme habitat. Marine mucilage characterize aquatic systems with altered environmental conditions. We investigated, by means of molecular techniques, viruses and prokaryotes within the mucilage and in surrounding seawater to examine the potential of mucilage to host new microbial diversity and/or spread marine diseases. We found that marine mucilage contained a large and unexpectedly exclusive microbial biodiversity and hosted pathogenic species that were absent in surrounding seawater. We also investigated the relationship between climate change and the frequency of mucilage in the Mediterranean Sea over the last 200 years and found that the number of mucilage outbreaks increased almost exponentially in the last 20 years. The increasing frequency of mucilage outbreaks is closely associated with the temperature anomalies. We conclude that the spreading of mucilage in the Mediterranean Sea is linked to climate-driven sea surface warming. The mucilage can act as a controlling factor of microbial diversity across wide oceanic regions and could have the potential to act as a carrier of specific microorganisms, thereby increasing the spread of pathogenic bacteria.
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Climate Change and the Potential Spreading of Marine
Mucilage and Microbial Pathogens in the Mediterranean
Sea
Roberto Danovaro
1
*, Serena Fonda Umani
2
, Antonio Pusceddu
1
1Department of Marine Sciences, Polytechnic University of Marche, Ancona, Italy, 2Department of Life Sciences, University of Trieste, Trieste, Italy
Abstract
Background:
Marine snow (small amorphous aggregates with colloidal properties) is present in all oceans of the world.
Surface water warming and the consequent increase of water column stability can favour the coalescence of marine snow
into marine mucilage, large marine aggregates representing an ephemeral and extreme habitat. Marine mucilage
characterize aquatic systems with altered environmental conditions.
Methodology/Principal Findings:
We investigated, by means of molecular techniques, viruses and prokaryotes within the
mucilage and in surrounding seawater to examine the potential of mucilage to host new microbial diversity and/or spread
marine diseases. We found that marine mucilage contained a large and unexpectedly exclusive microbial biodiversity and
hosted pathogenic species that were absent in surrounding seawater. We also investigated the relationship between
climate change and the frequency of mucilage in the Mediterranean Sea over the last 200 years and found that the number
of mucilage outbreaks increased almost exponentially in the last 20 years. The increasing frequency of mucilage outbreaks is
closely associated with the temperature anomalies.
Conclusions/Significance:
We conclude that the spreading of mucilage in the Mediterranean Sea is linked to climate-driven
sea surface warming. The mucilage can act as a controlling factor of microbial diversity across wide oceanic regions and
could have the potential to act as a carrier of specific microorganisms, thereby increasing the spread of pathogenic bacteria.
Citation: Danovaro R, Fonda Umani S, Pusceddu A (2009) Climate Change and the Potential Spreading of Marine Mucilage and Microbial Pathogens in the
Mediterranean Sea. PLoS ONE 4(9): e7006. doi:10.1371/journal.pone.0007006
Editor: Zoe Finkel, Mt. Alison University, Canada
Received June 23, 2009; Accepted July 27, 2009; Published September 16, 2009
Copyright: ß2009 Danovaro et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work has been funded by the SESAME project (EU Contract No. GOCE-2006-036949). The funders had no role in study design, data collection and
analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: r.danovaro@univpm.it
Introduction
Marine snow (i.e., amorphous aggregates with a size ranging from a
few millimetres to several metres) is ubiquitous in the oceans of the
World [1]. Water column stratification under summer conditions
favours the progressive coalescence of small-sized aggregates into large
massive sheets, thin layers, flocs and clouds, which are collectively
known as marine mucilage [2]. Mucilage is a gelatinous evolving stage
of marine snow (Figure 1), which can reach huge dimensions and
cover areas of hundreds of kilometres of coastline [3–6].
Mucilage is made of exopolymeric compounds with highly
colloidal properties that are released by marine organisms [7]
through different processes, including phytoplankton exudation
of photosyntetically-derived carbohydrates produced under
stressful conditions [8,9] (e.g., P-limited diatoms that produce
large amounts of polysaccharides [10–14]) and through death
and decomposition of cell-wall debris [15,16]. Such a release can
be coupled with a limited ability of prokaryotes to hydrolyze
these exopolymers by means of extracellular enzymes [17–18]
leading to the release and accumulation of large molecular
weight compounds in the system [19–26]. These processes can be
associated with viral infections of prokaryotes and phytoplankton
and the consequent cell lysis (viral shunt), which further
contributes to release and accumulation of dissolved organic
matter in the water column [27–31]. Whatever the causes
triggering the formation of marine mucilage, this phenomenon
has created increasing concern in coastal areas due to its socio-
economical consequences.
Worldwide the highly productive and shallow Adriatic Sea (and
particularly its Northern portion) within the Mediterranean basin
is the area most severely affected by the outbreak of massive
marine mucilage. Mucilage was reported here for the first time in
1729, and was originally described as a ‘‘dirty sea’’ phenomenon
(‘‘mare sporco’’) because it causes the clogging of fishing nets [32].
Since then, the presence of mucilage has been reported
sporadically, but in the last three decades, the frequency of this
phenomenon appears to have increased considerably [2]. The
presence of mucilage makes the seawater unsuitable for bathing
because of the bad smell produced, and the adherence of the
mucilage on the skin of bathers. Marine mucilage floating on the
surface or in the water column can display a long life span (up to
2–3 months) and once settled on the sea bottom, these large
aggregates coat the sediments, extending in certain cases for kms
and causing hypoxic and/or anoxic conditions [2]. The conse-
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quent suffocation of benthic organisms (including bottom-
associated nekton) [24] provokes serious economical damage to
tourism and fisheries [33].
In the present study we hypothesized that: i) marine mucilage
can represent a new, though ephemeral, substrate for microbial
colonization, including pathogenic forms, ii) increasing frequency
Figure 1. Mucilage and the ‘‘mare sporco’’ (dirty sea) phenomenon. Image of mucilage in surface off-shore waters (A) and in an advanced
stage of coalescence, after sampling (B).
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of mucilage outbreaks in the Mediterranean Sea is linked to recent
climate change and iii) increasing occurrence of marine mucilage
can increase spreading of marine diseases.
Results
Viruses and prokaryotes associated with marine mucilage
The microscopic analyses we conducted on samples of marine
mucilage revealed the presence of huge prokaryotic and viral
abundances (on average 3.7662.53 10
6
cells and 1.1160.26
10
9
viruses mL
21
). Prokaryotic and viral abundances in mucilage
were significantly higher (ANOVA P,0.001) than in surrounding
seawater (Figure 2A). Molecular analyses demonstrated the
presence of a huge bacterial diversity within the mucilage, with
a number of ribotypes significantly higher (approximately double;
ANOVA P,0.01) than in surrounding seawater (Figure 2B and
2C). The number of bacterial taxa encountered in the mucilage
matrix contributed for ca 68% to the total number of bacterial
taxa identified. We found that more than 90% of the bacterial taxa
encountered in the mucilage were not found in the surrounding
seawater.
Molecular analyses based on fluorescent in situ hybridization
revealed that mucilage contained a large number of pathogenic
bacteria (Figure 2D). The abundance of coliforms per unit of
volume in marine mucilage per unit of volume was four orders of
magnitude higher than in surrounding seawater, and Vibrio spp.
were significantly more abundant than in the water column
(ANOVA, p,0.01). The use of molecular fingerprinting tech-
niques (ARISA) carried out both on mucilage and on the
surrounding seawater provided evidence that mucilage aggregates
not only entrap prokaryotes present in the water column, but also
contain bacterial species (Escherichia coli and Vibrio harveyi), which
were absent in surrounding seawater.
Frequency and distribution of mucilage outbreaks
Analysis of historical reports indicated that the frequency of the
mucilage has increased almost exponentially in the last two
decades in the Mediterranean Sea (Figure 3). Prior to 1920
mucilage events have been reported only in the Adriatic Sea. Since
1980 mucilage events were also reported from the Aegean,
Northern and Tyrrhenian Seas. In the last 30 years the area with
the highest number of mucilage outbreaks was the Adriatic Sea
(n = 14) followed by the Tyrrhenian Sea (n = 11), and the Aegean
Sea (n = 9).
The analysis of temperature anomalies over the last 60 years
revealed that these have remained constantly positive since 1977
with values ranging from 0.097 (1986) to 0.524 (1998). Mucilage
occurrence displayed a significant relationship (Spearman Rank
correlation r
s
= 0.50, P,0.003; n = 34) with climate change (as
temperature anomalies, annual average; www.cpc.noaa.gov) in the
last 60 years.
Discussion
Mucilage as potential carriers of marine diseases
Mucilage is able to entrap high abundances of a wide range of
organisms from small phytoplankton to large zooplankton, and is
capable of scavenging plankton and detrital particles suspended in
the water column [34,35]. Our results provide evidence that
marine mucilage is also a major repository for prokaryotes and
viruses, which displayed a concentration factor (as ratio between
abundance in mucilage: abundance in seawater per unit of
volume) ranging from 10
3
–10
4
. No other organisms entrapped in
the mucilage were as enriched. The huge abundance of
prokaryotes and viruses within the mucilage could be due to the
ability of these large aggregates to entrap into free-living viruses
and prokaryotes from the water column. In addition the mucilage
represents a source of organic molecules potentially utilizable for
sustain prokaryotic metabolism and growth. Typically viral and
prokaryotic abundances in aquatic systems co-vary [23]. This also
Figure 2. Microbial abundance and diversity in marine
mucilage and surrounding seawater. (A) viral and prokaryotic
abundance; (B) bacterial diversity (as OTU, Operational Taxonomic
Units); (C) electropherograms of DNA extracted from a mucilage sample
and surrounding seawater; (D) number of pathogens. Panel B illustrates
diversity of bacterial assemblage: species in common are represented
using the same colour. In Panel C, each peak corresponds to an interval
of 62 base pairs, is assumed to represent a different OTU, and the
height of the peak is assumed to represent the quantity of each single
OTU.
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occurred in marine mucilage where a significant correlation
between prokaryote and viral abundance was observed (Spear-
man-rank correlation, r
s
= 0.99; p,0.001). The values of the ratio
of virus-to-prokaryotic abundance in the mucilage (always .17)
were significantly higher than values typically reported for
seawater [36], suggesting that mucilage can be characterized by
a strong viral shunt with a much higher probability of virus-host
contact than in surrounding seawater [37]. Similar values have
been recently reported for deep-benthic marine systems, where a
viral shunt proved to be extremely important [38]. The high viral
abundance can influence prokaryotic dynamics by killing the
prokaryotes and causing the release of particulate and dissolved
organic material, which can then contribute to the renewal and
persistence of the mucilage [23].
The use of fingerprinting techniques indicated that marine
mucilage is also a hot spot of bacterial diversity. The number of
ribotypes in the mucilage was on average ca 65% higher than in
the surrounding seawater. Since mucilage can remain suspended
in the seawater for months, it is possible that several prokaryotic
species are released in areas far from their origin during dispersal
of mucilage by currents.
Most known diseases affecting both marine invertebrate and
vertebrates, such as those referred to as yellow blotch, dark spots,
and the so-called rapid tissue necrosis, are only described for their
symptoms and have not been characterized by their aetiology or
pathogenesis [39]. Detailed microbiological investigations of
marine pathogens have been hampered previously by the
difficulties in cultivating them. Only recently has the development
of molecular methodologies allowed progress [40]. In the present
study, the use of molecular techniques such as the fluorescence in
situ hybridization (FISH) revealed the presence of a conspicuous
number of pathogenic bacteria (e.g., Vibrio harveyi) in the mucilage,
but not in surrounding seawater, which have the potential to infect
a wide range of organisms [41].
FISH analyses revealed also the presence of very high
abundances of total Coliforms and E. coli, which are common
indicators for the potential presence of pathogens. The presence of
these bacteria in the aggregates suggests that mucilage could have
potentially negative consequences on human health. The abun-
dance of these bacteria are typically monitored in coastal
environments as they are indicators of water quality and their
presence above certain threshold levels limits recreational activities
at sea. The ability of mucilage to potentially concentrate high
abundances of pathogenic bacteria is consistent with the
appearance of dermatitis and other syndromes associated to
human contact with the mucilage [42].
Although the mechanisms by which the mucilage hosts large
numbers of pathogens are not entirely clear, it might be
hypothesized that the complex organic matrix of the mucilage
offers micro-niches to pathogens with favourable conditions for
their colonization and survival [43]. Results reported here also
suggest that if the expansion of the mucilage occurrence will
continue in the future, it could be associated with increased
outbreaks of diseases caused by the potential release of large
numbers of pathogenic bacteria from the mucilage.
Mucilage and climate change
The analysis of historical reports in the Mediterranean Sea
indicates that the occurrence of mucilageeventsisincreasingand
spreading to several regions beyond the Adriatic Sea, where it
was documented for the first time. Mucilage is not closely
associated with the presence of eutrophic conditions, as several
mucilage outbreaks have been recently observed in oligotrophic
seas, such as the Aegean Sea. Moreover, the frequency of
mucilage outbreaks in the Adriatic Sea has increased in the last 2
decades concurrently with a significant decrease in primary
production. Furthermore there is no correlation between the
numberofmucilagerecordsperdecadeandthedecadalmeanof
Po river annual discharge in the Adriatic Sea (Spearman
r
s
=20.333; not significant, data not shown). It therefore can
be hypothesised that the expansion of mucilage outbreaks in
different areas of the Mediterranean Sea (including coastal
regionsthathavenopreviousrecordsforthisphenomenon,such
as the Marmara Sea [44]) do not result from increased primary
productivity of the system (i.e., eutrophication).
Although recent studies have suggested that a climatic shift
occurred in 1987 in the Mediterranean (e.g. the so called East
Mediterranean Transient [45] could have been responsible for a
shift in ecosystem functioning [46]), the linkage between mucilage
occurrence and climate change has been almost completely
neglected. Our analysis based on a record of approximately 60
years of mucilage appearance in the Mediterranean Sea (1950–
2008) has revealed that patterns of climate anomalies (e.g., the
positive anomaly of the surface temperature) explained a large
proportion of variance in mucilage outbreaks, on an annual and
decadal basis (Figure 4).
Figure 3. The areas in the Mediterranean Sea where the mucilage has been documented and the years of appearance.
doi:10.1371/journal.pone.0007006.g003
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The hypothesis of a link between mucilage formation and climate-
driven temperature anomalies is suggested by the apparent progressive
extension of the duration of this phenomenon. In the Adriatic Sea, for
instance, marine aggregates generally appear from May to July and
evolve into mucilage through the Summer (with a peak in August).
Recently (i.e., in 2003, 2006, 2007 and 2008), mucilage has appeared
much earlier (first recorded in November/December and January,
depending upon the area). The Winter 2006–2007 was the warmest
over the last 30 years, with average temperatures up to 2–3uCabove
the previous mean temperatures (http://www.noaanews.noaa.gov/
stories2007/s2798.htm), and the spatial extent and persistence of
mucilage reached unprecedented levels. In March 2007, for instance,
marine mucilage was seen to stretch along more than 2,500 km of the
Italian coastline. Massive aggregates lasted, almost continuously, for
more than five months. The last outbreaks have been reported in
autumn of 2008. This tendency, however, needs to be monitored in
thefutureforconsistency.
The presence of temperature anomalies alone cannot be used to
predict the occurrence of mucilage phenomenon on a basin scale
because several other (local) factors may promote the mucilage
formation and/or increases in the magnitude of this phenomenon
including the hydrodynamic regime (i.e., current speed and water
mass turnover), oxygen availability, and other factors. However,
the link between climate anomalies and the occurrence of
mucilage is evident and, in the light of the warming trend of the
Mediterranean Sea [47], the mucilage phenomenon could
increase in the future.
The coastal areas of the Mediterranean Sea that are repeatedly
affected by mucilage appearance share many common environ-
mental problems. Most of these systems have a long history of
human exploitation [48,49], including over-fishing (which through
trawling can be also responsible for the alteration of the benthic
biogeochemical cycles) [50], presence of macro- and micro-
pollutants (which can have a strong impact on microbial-loop
functioning and cause the increase of viral infection [51] or the
outbreak of microbial diseases [52] and altered ecosystem
functioning. Perhaps the misuse of these coastal environments
might exacerbate this phenomenon. Mucilage, in turn, can induce
Figure 4. Relationships between mucilage occurrence in the Mediterranean Sea and climate change (as magnitude of the thermal
anomalies) on (A) annual basis, (B) decadal basis. Annual and decadal temperature anomalies were retrieved from www.cpc.noaa.gov. Records
of mucilage appearance in the Mediterranean Sea are detailed in Text S1.
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hypoxic phenomena and even promote extensive anoxia [53]
resulting in a decreased production of ‘‘ecosystem goods and
services’’[54], and a lower ecosystem resiliency (ability to recover
after adverse impacts).
If the mucilage phenomenon continuous to increase in
frequency and duration, and to spread around the coastal areas
of the Mediterranean Sea, an increased frequency and extension
of some marine diseases may result with potential consequences to
human health [55]. In the past, the ‘‘Vibrio cholerae paradigm’’ has
represented the first important example of the cascade effects of
climate change on human health [56]. Vibrio cholera, indeed, lives
attached to the exoskeleton of marine copepods, which depend on
phytoplankton blooms for their nutrition. These in turn are
influenced by climate change [56]. We propose mucilage as a
potentially novel paradigm of the ecosystem alteration caused by
the synergistic effect of climate change and misuse of marine
resources. Mucilage on one hand represents symptomatic response
of the marine ecosystem to direct and indirect anthropogenic
impacts, and on the other a potentially expanding carrier of viruses
and bacteria, including pathogenic forms that are harmful for the
health of humans and marine organisms.
Methods
Sampling
Samples of seawater and mucilage were collected from coastal
waters of the Adriatic Sea in 2007 by means of sterilized Niskin
bottles and by 100 mL syringes operate by SCUBA divers,
respectively. Fifty mL each of mucilage and seawater were
immediately stored at 220uC for subsequent viral and prokaryotic
counts (within 48 h). Additional water samples were filtered on
0.2-mm pore-size polycarbonate filters and immediately processed
together with fresh mucilage samples for DNA extraction.
Viral and prokaryotic abundance and biodiversity in
seawater and mucilage
Viral and prokaryotic abundances were determined by
epifluorescence microscopy after staining with SYBR Green I
and normalised to mL of seawater or mucilage [37].
Automated rRNA Intergenic Spacer Analysis (ARISA) was
carried out on seawater and mucilage samples. DNA was extracted
from mucilage samples (ca. 1 mL) by means of the UltraClean Soil
DNA Isolation kit (MoBio Laboratoires Inc., California, USA)
[57]. Extracted DNA was determined fluorometrically using
SYBR Green I (Molecular Probes, USA) and quantified using
standard solutions of genomic DNA from E. coli [58]. The DNA
was then amplified using universal bacterial primers 16S-1392F
(59-GYACACACCGCCCGT-39) and 23S-125R (59-GGGTT-
BCCCCATTCRG-39), which amplify the bacterial ITS1 region
in the rRNA operon plus ca. 282 bases of the 16S and 23S rRNA.
The reverse primer 23S-125R was fluorescently labelled with the
fluorochrome HEX (MWGspa BIOTECH). PCR reactions were
performed in 50-ml volumes in a thermalcycler (Biometra,
Germany) using the MasterTaqHkit (Eppendorf AG, Germany).
30 PCR-cycles were used, consisting of 94uC for 1 minute, 55uC
for 1 minute and 72uC for 2 minute, preceded by 3 minutes of
denaturation at 94uC, followed by a final extension of 10 minutes
at 72uC. To check for eventual contamination of the PCR
reagents, negative controls containing the PCR-reaction mixture
but without the DNA template were run during each PCR
analysis. Positive controls, containing genomic DNA of Escherichia
coli, were also used. PCR-products were checked on agarose-TBE
gel (1%), containing ethidium bromide for DNA staining and
visualization. For each mucilage sample, two different PCR
reactions were run and then pooled together to minimize
stochastic PCR biases. This process was carried out in duplicate,
for a total of 4 different PCR reactions for each sample. The two
resulting PCR combined products were then purified using the
Wizard PCR clean-up system (Promega, Wisconsin, USA),
resuspended in 50 ml of milliQ water supplied with the clean-up
system and then quantified spectrofluorimetrically as described
above. For each ARISA analysis, about 5 ng of amplicons were
mixed with 14 ml of internal size standard (GS2500-ROX; Applied
Biosystems, Foster City, Calif.) in deionized formamide, then
denatured at 94uC for 2 minutes and immediately chilled in ice.
Automated detection of ARISA fragments was carried out using
an ABI Prism 3100 Genetic Analyzer (Applied Biosystems).
ARISA fragments in the range 390–1400 bp were determined
using Genescan analytical software 2.02 (ABI). Bacterial phylo-
type/genotype richness was expressed as the total number of peaks
within each electropherogram.
Identification of pathogens by Fluorescent In Situ
Hybridization (FISH)
For the detection and enumeration of potentially pathogenic
microorganisms (i.e. total Coliforms, Escherichia coli,Vibrio spp. and
Vibrio harveyi) we used the FISH (Fluorescent In Situ Hybridization)
technique targeting the bacterial 16S rRNA. From each sample,
ca. 1 mL of each mucilage sample was fixed in replicate in a 1:1
sterile solution of PBS:ethanol and sonicated three times. Aliquots
of each sample were then properly diluted and filtered through
0.2 mm black polycarbonate filters (Nuclepore). The filters were
then hybridized using Cy3-labeled probes under appropriate
hybridization condition for each probe and washed using
appropriate washing buffers. Then, each filter was counterstained
with DAPI (0.5 mgmL
21
), mounted onto microscopic slides and
observed under epifluorescence microscopy. We used the probes
‘‘D’’, Colinsitu, GV, VH-2 for counting Total Coliforms, Escherichia
coli,Vibrio spp., and Vibrio harveyi, respectively.
Historical data collection and statistical analyses
For the purposes of this research, we searched for mucilage and
macro-aggregate (.500 mm in size) records in oceans worldwide
in published literature (Sciencedirect, ASFA). The research for
mucilage records was also extended to include the whole of the
Internet, to identify events not documented in scientific papers
(Table S1). Annual mean data on Po river discharge (1990–2007)
in the Adriatic Sea have been extracted from the Hydrological
Annales of the Regional Agency for Prevention and Climate of the
Emilia Romagna Region (www.arpa.emr.it).
Quantitative differences in microbial variables between muci-
lage and seawater samples were tested using one-way analysis of
variance (ANOVA). The type of substrate (mucilage vs. seawater)
was treated as a fixed factor with two levels and significant
differences were also assessed using a post-hoc Student-Newman-
Kuels’ test (SNK). ANOVA and SNK tests were carried out using
the software GMAV 5.0 (University of Sidney, Australia). The
relationships between microbial variables within mucilage samples
and within seawater were tested using a Spearman-rank
correlation analysis.
Supporting Information
Table S1 List of the records of the appearance of mucilage in
the Mediterranean Sea and specific geographic locations.
Found at: doi:10.1371/journal.pone.0007006.s001 (0.08 MB
DOC)
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Text S1 This file contains all info collected on historical events of
mucilage appearance in the Mediterranean Sea.
Found at: doi:10.1371/journal.pone.0007006.s002 (0.07 MB
DOC)
Acknowledgments
Authors are grateful to G.M. Luna for support in the analyses of molecular
fingerprinting and to C. Corinaldesi (Polytechnic University of Marche) for
useful suggestions. Two anonymous reviewers are thanked for precious
comments on the manuscript.
Author Contributions
Conceived and designed the experiments: RD AP. Performed the
experiments: RD AP. Analyzed the data: RD AP. Wrote the paper: RD
SFU AP.
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Spreading Marine Mucilage
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... For instance, mucilages have appeared more frequently (associated with a malfunctioning of the microbial loop) in the Adriatic Sea, where it was documented for the first time, and in several regions beyond, in recent decades, concomitantly with a significant increase in sea surface temperature (Danovaro et al. 2009). Mucilage is not closely associated with the presence of eutrophic conditions, as several mucilage outbreaks have been recently observed in oligotrophic seas, such as the Aegean Sea (Danovaro et al. 2009). ...
... For instance, mucilages have appeared more frequently (associated with a malfunctioning of the microbial loop) in the Adriatic Sea, where it was documented for the first time, and in several regions beyond, in recent decades, concomitantly with a significant increase in sea surface temperature (Danovaro et al. 2009). Mucilage is not closely associated with the presence of eutrophic conditions, as several mucilage outbreaks have been recently observed in oligotrophic seas, such as the Aegean Sea (Danovaro et al. 2009). The Ligurian Sea, one of the coldest areas of the Mediterranean Sea, displays a low number of subtropical species and a higher abundance of cold-temperate water species. ...
... The outbreaks of this species, along with other jellyfish species, may become more frequent in the Mediterranean Basin in the future and extend over a longer period of the year than previously, causing changes to the pelagic food web and thereby reducing fishery production . Rising seawater temperatures might also trigger the increased spread of pathogens throughout the Mediterranean in the future, affecting both marine organisms, and human health (Danovaro et al. 2009) (see Section 5.2.3 on heat-related impacts). ...
Technical Report
Full-text available
Balzan MV, Hassoun AER, Aroua N, Baldy V, Bou Dagher M, Branquinho C, Dutay J-C, El Bour M, Médail F, Mojtahid M, Morán-Ordóñez A, Roggero PP, Rossi Heras S, Schatz B, Vogiatzakis IN, Zaimes GN, Ziveri P 2020 Ecosystems. In: Climate and Environmental Change in the Mediterranean Basin – Current Situation and Risks for the Future. First Mediterranean Assessment Report [Cramer W, Guiot J, Marini K (eds.)] Union for the Mediterranean, Plan Bleu, UNEP/MAP, Marseille, France, pp. 323-468.
... The causes of the mucilage events are still under debate whether they are initiated by eutrophication due to increased anthropogenic/natural nutrient inputs or they are related to the temperature increases due to the climate change and its consequences on the physicochemical properties of seawater (Danovaro et al., 2009). In general, mucilage phenomenon is related to coupling effects between seawater organic matter production and the meteorological and oceanographic conditions (De Lazzari et al., 2008). ...
... In general, mucilage phenomenon is related to coupling effects between seawater organic matter production and the meteorological and oceanographic conditions (De Lazzari et al., 2008). Strong correlations were found between the annual average temperatures and the mucilage events between 1870 and 2010 were previously linked to the influence of climate change on the frequency of mucilage formation (Danovaro et al., 2009). In addition, sea surface temperature (SST) is another factor for the mucilage formation. ...
... In addition, sea surface temperature (SST) is another factor for the mucilage formation. In this scope, the relation between the mucilage events and increased SSTs in Mediterranean Sea was shown in recent studies (Danovaro et al., 2009;Savun-Hekimoğlu & Gazioğlu, 2021). Tuzcu Kokal et al. (2021) detected SST anomalies in the Sea of Marmara based on NOAA satellite data from 1970 to 2021 and found an increasing trend in SST, which may likely provided the conditions for mucilage aggregation. ...
Article
Full-text available
Marine mucilage outbreaks occurred in the Sea of Marmara in 2021 which severely affected the marine ecosystem. The thick mucilage blankets with different colors became a public concern due to the toxicity potential related to pathogens that accumulate in prolonged presence of mucilage. The mucilage-covered areas in the Sea of Marmara detected by remote sensing data acquired in 2021 were previously reported. However, the areal extents and spectral characteristics of the different colored mucilage types remain unknown. This study presents the spectral characteristics of different types of mucilage in the İzmit Bay in the Sea of Marmara by using medium- (Sentinel-2) and high-spatial resolution (Worldview-3) satellite images. Also, the sea surface temperatures (SST) were studied in relation with the mucilage formation from January 2015 to August 2021 by using NOAA data. Two multispectral satellite sensors Sentinel-2 and Worldview-3 were studied for their potential for mucilage mapping and characterization in the sub-region İzmit Bay. Support vector machine (SVM) classifier was used to detect three different types of mucilage with distinguishable spectral differences in infrared region ranging from 725 to 950 nm. Three different types of mucilage were characterized based on color and texture including (a) the white mucilage aggregates with dispersed patterns which are likely freshly formed, (b) the yellow mucilage accumulations in the coasts that are wind/current transported, and (c) the brown mucilage accumulations that are probably the most-aged. Our results showed that brown mucilage and white mucilage showed similar reflectance values between 425 and 545 nm region, while yellow mucilage showed higher and more distinctive spectral reflectance than white and brown mucilages. The NOAA data showed that average surface water temperature has been increased over the years from 2015 (16.1 °C) to 2021 (17.6 °C). This increase trend in SSTs points out a likely relation with the mucilage formation and hence may suggest a potential of repeating mucilage events in the near future. This study provides a practical methodology for monitoring, classification, and efficient site selection for mucilage cleaning areas in the Sea of Marmara.
... Although the phenomenon of sea snot and the reasons for its occurrence is a complex subject, it can be said that sea snot is mostly composed of organic structures consisting of a mixture of carbohydrates and proteins (Yücel et al. 2021). Danovaro et al. 2009 stated that the sea snot formation event that occurred in the sea in the Turkish Mediterranean some time ago actually started in the early 1700s which occurred in the Sea of Marmara in September-October 2007 (Aktan, 2008). As recently as December 2020, sea snot formation was scientifically recorded in Turkey's Anakkale Strait above an assemblage of hard, gorgonian, coralligenous, and spongy corals (Özalp 2021). ...
... The presence of these bacteria is not only caused by the natural eutrification process, but can also be caused by external pollutants. Eutrophication that occurs causes nutrient enrichment which if excessive can cause the formation of biomass in the form of jelly (Danovaro, R., et al. 2009). The biomass can be in the form of polysaccharides and proteins with estimates containing bacteria, pathogenic viruses known as sea snot (Keleş, G., et al, 2020), or contain abundant phytoplankton which can be dangerous in the form of Harmful algae blooms (HAB) (Young CS). ...
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The incident that occurred some time ago in Bima Bay, West Nusa Tenggara Province, which began to be seen on April 25/26 2022 is a phenomenon that is quite horrendous for residents of the City/Regency of Bima and outside the Bima area. According to several preliminary studies based on laboratory tests and local inspections, it is estimated that there are three possible causes, namely: (1) Sea Snot, (2) Algae Explosion and Metabolism (Algae Blooms) and (3) Oil Spill (Algae Blooms). oil spill). This study aims to examine the assessment of the sea on human health and welfare, in particular to examine the causes of seawater phenomena that occur in Bima Bay by considering many aspects. This study identifies and makes estimates based on data and facts that relate the phenomena that occur/pollutants to health effects on marine biota and on humans. It was carried out by observing the quality of sea water in Bima Bay based on the results of several laboratory tests on specimens taken on 27-29 April 2022. The test results of sea water samples taken on 27 April 2022 showed a high nitrate content. levels of 9.75 mg/l to 34.75 mg/l (water quality standard for nitrate content = 0.008 mg/l) and accompanied by an increase in ammonia level of 0.41 mg/l (water quality standard for ammonia content = 0, 3 mg/l) l). l) and phosphate content of 0.06-0.08 mg/l (Phosphate quality standard = 0.015 mg/l). Total ammonia, nitrate and phosphate are environmental parameters that contain nutrients which if present in high concentrations and even continue to increase in marine waters will cause eutrophication (bloom) which can be very dangerous for other marine biota by causing a decrease in dissolved oxygen, plankton growth which can cause decrease in fish population, bad smell, and bad taste and can cause the formation of biomass in the form of jelly. The biomass can be in the form of polysaccharides and proteins with an estimated containing bacteria, viral pathogens known as sea snot.
... Musilaj olayı, Marmara Denizi'nde bilinen bir hadise olmasıyla birlikte, dünyanın farklı denizlerinde gerçekleştiği bildirilmiştir [11]. Akdenizde musilaj olayının varlığı ise 18. yüzyıldan bu yana rapor edilmektedir [12]. Bunun yanında son yıllarda musilaj olayının oldukca sık rapor edilir bir dinamik kazandığı da bilinmektedir [6]. ...
Article
Musilaj olayı denizlerin abiyotik faktorlerinde önemli değişiklikler oluşturmanın yanında, canlılık için de önemli tehditler oluşturmaktadır. Oluşturduğu bu önemli etkiler göz önünde bulundurulduğunda musilaj olayının mekansal ve zamansal oluşumunu hızlı şekilde tespit ve takip etmek önem kazanmaktadır. Bu çalışmada, musilaj olayının gerçekleştiği deniz alanlarının hızlı tespitine yönelik olarak atmosfer üstü sudan çıkan radyans reflektans değerleri üzerinde oluşturduğu optik olarak tanımlayıcı motif tespit edilmesi amaçlanmıştır. Bulgular, musilaj olayının gözlemlendiği deniz alanlarının diğer alanlara göre on ila yedi kat arasında daha yüksek atmosfer üstü sudan çıkan radyans reflektans değerlerine ulaştığı tespit edilmiştir. İstatistiki olarak anlamlı bu farkın optik tanımlayıcı motifi olarak tanımlanması mümkün olmuştur. Ortaya koyulan bu motifin gerek musilaj hadisesinin erken tespiti, gerekse ulusal izleme sistemi oluşturmak konusunda önemli katkılar sağlayacağı düşünülmektedir.
... The first mucilage coverage in The Sea of Marmara was reported in 2007 [1,2]. Now, mucilage, also known as sea snot, is spreading again along the Sea of Marmara, and although the coastal municipalities are in cooperation to clean up the waters, it occurs again after some days [3,4,5]. Recovering from mucilage may take months, and then seeking out the right cleaning up techniques may take even longer. ...
... Both sessile and mobile marine creatures have been found to congregate in seawater connected parts of the ships (Lee and Chown 2007;Frey et al. 2014). Barnacles, bryozoans, sea stars, polychaetes, gastropods, ascidians, hydroids, seagrass, amphipods, mytilus galloprovincialis, algae, hydroids, caprella mutica, crustaceans, molgula and bivalves are some of proliferating and harmful marine creatures associated with ship sea chests (Lee and Chown 2007;Ashton et al. 2007;Coutts and Dodgshun 2007;McDonald 2012;Frey et al. 2014) Specifically, mucilage is one of the mentioned clogging materials which has become increasingly common in some narrow sea channels in recent years, owing to the effects of global warming (Danovaro, Fonda Umani, and Pusceddu 2009;Tas, Kus, and Yilmaz 2020). On the other hand, there may be inanimate pollutants such as sediment and human-derived materials that cause fouling or blockage in sea chests. ...
Article
Sea pollution has negative consequences and has an impact on the marine ecosystem and ship machinery processes. The main risk of sea pollution on ship is based on sea chests that are used for ballast water and firefighting. In addition to this, sea chest fouling, which primarily forms as a result of pollution, has an impact on the ship machinery, navigation in waterways, and the environment. The possibility of failure related to sea chest fouling issues in seawater cooling systems used to cool ship machinery parts were investigated in this study. Significant defects in the cooling and related engine systems were determined using both a full-mission Kongsberg engine room simulator (ERS) process and failure modes and effects (FMEA) technique, which relied on expert judgments within the cause–effect relationship. According to the findings, sea chest pollution has a direct impact on the ships’ cooling water systems and other related components, causes power losses, and leads the main engine to shut down, resulting in the ship losing maneuverability. As a result of these circumstances, the risk of catastrophic events such as grounding, contact, collision, flooding, fire explosion, and others was determined.
... • As a result of cell autolysis, the mixing and accumulation of organics in the cell contents into sea water (Danovaro et al., 2009). ...
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Coronavirus disease (Covid-19) has prompted many companies to change fundamentally the way of doing business accross different sectors and regions. Businesses suddenly implemented strategies to stay safe and help prevent the spread - work from home, restricted in-person business operations, physical distancing, limited number of physically present workforce, to name but a few. Organizational performance has had an extremely important or fundamental role for the specialists in many fields (e.g. strategic planners, operations, finance, legal, and organizational development) even before the pandemic. Companies were looking for optimal strategic solutions to resume operations and carry on with serving their customers. This paper aims to examine the current situation faced by companies in North Macedonia in terms of measuring, managing and predicting organizational performance during the COVID-19 pandemic. In order to investigate the impact of COVID-19 outbreak on organizational performance, we have conducted 100 surveys of companies across the country. The results show that almost half of companies have adapted the measurements of organizational performances to the new conditions during the pandemic. Most respondents said they recognized the importance of organizational performance as a broad construct which captures what companies do, produce, and accomplish for the numerous constituencies with which they interact. In other words, it comprises the actual output or results of a business as measured against its intended outputs (or goals and objectives). Overall, organizational performance has generally decreased during the pandemic, with employees being the main determinant of organizational performance.
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Sea snot, which was seen and reported in the Adriatic and Tyrrhenian Seas in the early 1990s, had been on Turkey's agenda as an environmental massive disaster from the winter months of 2021 until the end of summer in the Sea of Marmara. Due to the magnitude and topicality of the subject, the samples collected from the coastal areas where sea snot is observed in Marmara from January until July were examined. According to the results obtained, 5 classes were determined in sea snot. Species of algae that secrete mucilage, which provides stickiness to the formation, were also been identified in sea snot. These are 1 dinoflagellate, 2 Prymnesiosides, 5 diatoms, and 2 cyanobacteria species. 8 toxic planktonic species were detected in sea snot: 1 causing PSP poisoning and 3 of dinoflagellate causing DSP poisoning; 1 of prymnesiophisid that releases ichthyotoxin to the sea environment, and 3 of diatoms that cause ASP poisoning.
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Various types of floating macroalgae and other floating matters have been reported in the global oceans and inland waters, and their remote detection has relied primarily on passive optical sensors. These sensors provide multiple spectral bands and frequent revisits, yet they all suffer from clouds. Synthetic aperture radar (SAR) imagers are active sensors that overcome this obstacle, yet their capacity in detecting macroalgae and other floating matters is generally unknown. Here, through statistical analysis and comparison of the Sentinel-2/MultiSpectral Instrument (MSI) and Sentinel-1/SAR imagery, we attempt to fill this knowledge gap. The types of floating matters considered in this study include macroalgae (Ulva Prolifera in the Yellow Sea, Sargassum horneri in the East China Sea, and Sargassum fluitans/natans in the Caribbean Sea), cyanobacteria (Microcystis, Nodularia spumigena, and Trichodesmium), dinoflagellates (green and red Noctiluca), organic matters (sea snots and brine shrimp cysts), and marine debris (driftwood). Of these, the only floating matter that can be definitively detected in Sentinel-1/SAR imagery is U. prolifera, followed by the occasional detection of S. fluitans/natans and driftwood. In all detection cases, the macroalgae features always appear in Sentinel-1/SAR imagery with positive contrast from the surrounding waters. Because of the all-weather measurements, SAR observations can therefore complement those from the optical sensors in monitoring and tracking U. prolifera and S. fluitans/natans in their respective regions.
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Aims: Bacterial response to temperature changes can influence their pathogenicity to plants and humans. Changes in temperature can affect cellular and physiological responses in bacteria that can in turn affect the evolution and prevalence of antibiotic-resistance genes. Yet, how antibiotic-resistance genes influence microbial temperature response is poorly understood. Methods and results: We examined growth rates and physiological responses to temperature in two species-E. coli and Staph. epidermidis-after evolved resistance to 13 antibiotics. We found that evolved resistance results in species-, strain- and antibiotic-specific shifts in optimal temperature. When E. coli evolves resistance to nucleic acid and cell wall inhibitors, their optimal growth temperature decreases, and when Staph. epidermidis and E. coli evolve resistance to protein synthesis and their optimal temperature increases. Intriguingly, when Staph. epidermidis evolves resistance to Teicoplanin, fitness also increases in drug-free environments, independent of temperature response. Conclusion: Our results highlight how the complexity of antibiotic resistance is amplified when considering physiological responses to temperature. Significance: Bacteria continuously respond to changing temperatures-whether through increased body temperature during fever, climate change or other factors. It is crucial to understand the interactions between antibiotic resistance and temperature.
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The depth-dependent, seasonal, and diel variability of virus numbers, dissolved DNA (D-DNA), and other microbial parameters was investigated in the northern Adriatic Sea. During periods of water stratification, we found higher virus abundances and virus/bacterium ratios (VBRs) as well as a larger variability of D-DNA concentrations at the thermocline, probably as a result of higher microbial biomass. At the two investigated stations, virus densities were highest in summer and autumn (up to 9.5 × 10(10) 1(-1)) and lowest in winter (< 10(9) 1(-1)); D-DNA concentrations were highest in summer and lowest in winter. The VBR as well as an estimated proportion of viral DNA on total D-DNA showed a strong seasonal variability. VBR averaged 15.0 (range, 0.9-89.1), and the percentage of viral DNA in total D-DNA averaged 18.3% (range, 0.1-96.1%). An estimation of the percentage of bacteria lysed by viruses, based on 2-h sample intervals in situ, ranged from 39.6 to 212.2% d(-1) in 5 m and from 19.9 to 157.2% d(-1) in 22 m. The estimated contribution of virus-mediated bacterial DNA release to the D-DNA pool ranged from 32.9 to 161% d(-1) in 5 m and from 10.3 to 74.2% d(-1) in 22 m. Multiple regression analysis and the diel dynamics of microbial parameters indicate that viral lysis occasionally could be more important in regulating bacterial abundances than grazing by heterotrophic nanoflagellates.
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The frequent discrepancy between direct microscopic counts and numbers of culturable bacteria from environmental samples is just one of several indications that we currently know only a minor part of the diversity of microorganisms in nature. A combination of direct retrieval of rRNA sequences and whole-cell oligonucleotide probing can be used to detect specific rRNA sequences of uncultured bacteria in natural samples and to microscopically identify individual cells. Studies have been performed with microbial assemblages of various complexities ranging from simple two-component bacterial endosymbiotic associations to multispecies enrichments containing magnetotactic bacteria to highly complex marine and soil communities. Phylogenetic analysis of the retrieved rRNA sequence of an uncultured microorganism reveals its closest culturable relatives and may, together with information on the physicochemical conditions of its natural habitat, facilitate more directed cultivation attempts. For the analysis of complex communities such as multispecies biofilms and activated-sludge flocs, a different approach has proven advantageous. Sets of probes specific to different taxonomic levels are applied consecutively beginning with the more general and ending with the more specific (a hierarchical top-to-bottom approach), thereby generating increasingly precise information on the structure of the community. Not only do rRNA-targeted whole-cell hybridizations yield data on cell morphology, specific cell counts, and in situ distributions of defined phylogenetic groups, but also the strength of the hybridization signal reflects the cellular rRNA content of individual cells. From the signal strength conferred by a specific probe, in situ growth rates and activities of individual cells might be estimated for known species. In many ecosystems, low cellular rRNA content and/or limited cell permeability, combined with background fluorescence, hinders in situ identification of autochthonous populations. Approaches to circumvent these problems are discussed in detail.
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The frequent discrepancy between direct microscopic counts and numbers of culturable bacteria from environmental samples is just one of several indications that we currently know only a minor part of the diversity of microorganisms in nature. A combination of direct retrieval of rRNA sequences and whole-cell oligonucleotide probing can be used to detect specific rRNA sequences of uncultured bacteria in natural samples and to microscopically identify individual cells. Studies have been performed with microbial assemblages of various complexities ranging from simple two-component bacterial endosymbiotic associations to multispecies enrichments containing magnetotactic bacteria to highly complex marine and soil communities. Phylogenetic analysis of the retrieved rRNA sequence of an uncultured microorganism reveals its closest culturable relatives and may, together with information on the physicochemical conditions of its natural habitat, facilitate more directed cultivation attempts. For the analysis of complex communities such as multispecies biofilms and activated-sludge flocs, a different approach has proven advantageous. Sets of probes specific to different taxonomic levels are applied consecutively beginning with the more general and ending with the more specific (a hierarchical top-to-bottom approach), thereby generating increasingly precise information on the structure of the community. Not only do rRNA-targeted whole-cell hybridizations yield data on cell morphology, specific cell counts, and in situ distributions of defined phylogenetic groups, but also the strength of the hybridization signal reflects the cellular rRNA content of individual cells. From the signal strength conferred by a specific probe, in situ growth rates and activities of individual cells might be estimated for known species. In many ecosystems, low cellular rRNA content and/or limited cell permeability, combined with background fluorescence, hinders in situ identification of autochthonous populations. Approaches to circumvent these problems are discussed in detail.
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The “successional stage” of marine aggregates from formation to final decay was investigated in the northern Adriatic Sea in summer 199 1. In marinc snow, bacterial biomass and production rates increased exponentially and in gellike aggregates (GEA-considered as late-stage marine snow) reached values 23 orders of magnitude higher than in ambient water. Specific growth rates of marine snow-associated bacteria (0.3 l-l .76 d -I) were similar to ambient water bacteria; however, they were significantly lower in GEA (0.08-0.3 1 d I). Concentrations of dissolved free amino acids (DFAA) in aggregates were up to 80 PM. Despite these high concentrations of DFAA, the organic C: N ratio increased significantly over the 3 months of the investigation period, ranging from 6.7 to 17.3 and indicating that refractory substances accumulate in aging aggregates. This notion is also supported by the ratio of a-glucosidase activity to P-glucosidase activity, which declined from ambient water (a-glue: ,&gluc = 1.7) to marinc snow and GEA (Cu-glut: fl-glut = 0.5 1). Extracellular enzymatic activity calculated on a per cell basis was similar for ambient water and marinc snow-attached bacteria, but significantly lower rates were obtained for GEA. These data indicate that GEA become an increasingly poor habitat for bacterial growth. The relation between hydrolysis rate and substrate uptake does not support the hypothesis of a loose coupling between hydrolysis and uptake in marine snow-attached bacteria.