Marine Climate Change in Australia

Impacts and Adaptation Responses 2012 REPORT CARD

Microbes
Nicole S. Webster1 and David G Bourne1

1
Australian Institute of Marine Science, PMB 3 Townsville, Queensland 4810, Australia
n.webster@aims.gov.au

Webster N.S. and Bourne D.G.. (2012) Microbes. In A Marine Climate Change Impacts and
Adaptation Report Card for Australia 2012 (Eds. E.S. Poloczanska, A.J. Hobday and A.J. Richardson).

Summary

Microorganisms are critical to all biogeochemical cycles and affect all living
organisms via their symbiotic and pathogenic partnerships. A fundamental question
for climate change scientists and marine microbiologists is what effects human
induced changes will have on the services marine microbes perform for the planet.
Whilst recent developments in technology have revolutionized our ability to
characterize and define microbial communities and greatly enhanced our
understanding of their functional roles and thresholds, we are still unable to measure
complex microbial processes in a way that allows scientists to incorporate microbes in
global climate models. In addition, Australia has a complete lack of long term data
sets on marine microbial community dynamics, making it impossible to infer the
potential impacts of climate change. Research on marine microbiology must therefore
rapidly accelerate in order to solve questions of how environmental shifts will change
microbial functioning and the subsequent impacts this will have on the ecosystems
they support.

Introduction

Microorganisms constitute the largest diversity and biomass of all marine biota yet
they are rarely considered in climate change reports. This is despite the fact that
microbes are central to the global cycles and therefore play a critical role in either
mitigating or exacerbating the effects of climate change. The phenotypic plasticity of
microbes and their ability to evolve rapidly also means they can rapidly shift their
metabolic capabilities, host range, function and community dynamics in response to
changing environmental conditions. To predict the response and resilience of marine
ecosystems and associated fauna subjected to environmental stress we therefore need
to understand how the diversity and function of these microorganisms is affected.
Historically, marine microorganisms have been overlooked due to their enormous
diversity, highly dynamic populations and lack of suitable methodology for
investigating the important functional roles they play at all levels of the marine
ecosystem. However, with advancing technologies it is now possible to explore the
role of individual microbes in the marine environment, though a lack of long term
datasets hinders our ability to predict potential climate impacts. Further complicating
our understanding is the fact that not all microbes function in the same way. For

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instance, some microbes are taking carbon dioxide out of the ocean whereas others are
producing it. Understanding the net effect of activities from these highly complex
communities and predicting how this will change under different environmental
conditions is an enormously difficult problem to solve.

“I make no apologies for putting microorganisms on a pedestal above all other living things.
For if the last blue whale choked to death on the last panda, it would be disastrous but not the
end of the world. But if we accidentally poisoned the last two species of ammonia-oxidisers,
that would be another matter. It could be happening now and we wouldn’t even know”
- From Tom Curtis (July 2006) in Nature Reviews Microbiology Vol 4, Issue 488

Marine microorganisms discussed in this report encompass a diverse array of

organisms including Bacteria, single celled phytoplankton (also in the Bacteria
domain), Archaea, and Viruses. In every litre of seawater approximately 1 billion
microbial cells are present and 10 billion viruses are estimated. Global oceanic
densities of microbes are estimated at 3.6 x 1029 bacterial cells (Sogin et al., 2006),
1.3 x 1028 archaeal cells (Karner et al., 2001) and 4 x 1030 viruses (Suttle, 2005).
These microorganisms are central to the global biogeochemical cycles (including C, N,
S, P, Fe and other trace elements) carrying out many of the transformations that other
organism cannot do, though which sustain life on our planet. Without the smooth
functioning of these biogeochemical cycles, life on this planet would cease to exist.
Therefore understanding how climate shifts affect marine microbial populations is
fundamental to identifying the risks we face into the coming century.

Diverse microbial communities inhabit all

areas of the marine biosphere. Fluorescent
DNA probing of bacteria within coral reef
biofilms reveals the complexity in community
structure. Currently, estimates of marine
bacterial diversity range from only a few
thousand species to as many as two million
distinct taxa (Curtis et al., 2002).

While microorganisms are important for maintaining the health of our marine
environments they can also have detrimental effects by causing disease outbreaks. In
recent decades, there has been a global increase in reports of disease in marine
organisms including fish, seals, dolphins, shellfish (oysters, scallops, abalone and
clams), starfish, urchins, sponges, seagrass, kelp, coralline algae and corals (Harvell et
al., 1999; Harvell et al., 2002; Lafferty et al., 2004; Bally and Garrabou, 2007;
Haapkyla et al., 2007; Webster, 2007). Determining if these reported outbreaks are
due to improved monitoring, changed environmental conditions, opportunistic or
emerging pathogens or reducing host resistance and resilience is extremely difficult.
Nevertheless, environmental drivers including rising SST and eutrophication are

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known to compromise the physiological fitness of coral reef organisms which is

believed to contribute to the increased prevalence of diseases globally.

Corals both locally and globally are being affected by a wide range of diseases
including Porites ulcerative white spot (left panel), tumours (middle panel) and
brown band (right panel).

Australia has no long-term records documenting marine bacterial, archaeal or viral

community dynamics and in fact very few such datasets exist globally. Though there
are temporal measurements from seawater stations at a number of sites around the
world such as the BATS (Sargasso Sea) and MANOA (Hawaii), the bulk of the data
collected at these sites focuses on physical and biogeochemical data. Temporal
records for prokaryotic communities exist for the English Channel and the Sargasso
Sea. The bacterioplankton communities at the temperate marine coastal site in the
English Channel were studied by high resolution 16S rRNA gene tag pyrosequencing
of samples taken monthly over 6 years. Whilst the data showed strong repeatable
seasonal patterns in the bacterial communities, little could be concluded about climate
change effects based on the limited time frame (Gilbert et al., 2012). Similarly, a
decade long high-resolution time-series from the upper 300m in the northwestern
Sargasso Sea revealed recurring temporal and vertical patterns of virioplankton
abundance which were highly correlated with the dominant picophytoplankton
lineage Prochlorococcus (Parsons et al., 2012). While these and other similar studies
provide the basis for long-term microbial data sets, we still need at least 30
consecutive years to recognize and predict long-term trends in relation to climate
shifts. In Australia, while seawater collection and monitoring sites have been set up
through the integrated marine observing system (IMOS), currently there is no analysis
of prokaryotic and viral populations to facilitate the detection of long term trends.
However, on a positive note, samples are being stored so there is still the possibility
for retrospective analysis.

Despite the overwhelming complexity of marine microbial communities and our

limited knowledge of the long term effects of climate change on these populations,
there are many advantages to including microbes in environmental stress assessments.
Marine microbes often have strict physiological thresholds that make them sensitive
to small changes in temperature, pH, nutrients, salinity and oxygen. Marine
microorganisms are also able to respond very rapidly to changing environmental
conditions, have the ability to rapidly evolve and can respond to small changes in
their environment by the expression of stress-regulated genes. These factors make

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them ideal bio-indicator organisms. Therefore, despite the lack of long-term data
records, if key organisms and their responses can be identified, it may be possible to
infer some of the effects of climate change.

Multiple stressors

Our ability to reliably assess the impacts of multiple stressors on marine microbial
populations is limited by a lack of data on the functional roles of most species
combined with the incredible complexity of marine microbial communities involved
in biogeochemical cycling and intimate (symbiotic / pathogenic) associations with
macroorganisms. Although this has not yet been examined, it is foreseeable that
multiple stressors such as a combination of elevated SST and nutrients /contaminants
from river discharge and land run-off may have compounding effects on microbial
communities at all levels of the ecosystem from bacterioplankton to biofilms and
symbiotic / pathogenic organisms. In addition, with such limited data on how marine
microbial communities respond to climate change parameters, it is difficult to
accurately assess if other environmental factors would confound detection of impacts
due to climate change. However, since microbes respond rapidly to any
environmental changes there is little doubt that such environmental noise would be
more problematic in coastal areas than open ocean regions. It would also be
reasonable to assume that concurrent stressors would have a more detrimental impact
on the ecosystem and potentially constrain the adaptive capacity of marine
microorganisms generally. The high sensitivity and relatively short generation times
of most marine microbes suggest that in the absence of multiple stressors, microbes
would be better able to adapt to chronic rather than acute environmental perturbations.
Concurrent stressors are probably also the most foreseeable threat to ecosystem
resilience. For example, an increase in seawater temperature and/or nutrient load has
a detrimental effect on the health of many invertebrate species making them more
susceptible to disease and increasing the potential for opportunistic bacterial species
to become pathogenic.

Observed impacts

Temperature
The sensitivity of most marine microbes (pelagic, benthic and symbiotic) to
temperature is extremely difficult to assess as precise thresholds are known for only a
few cultivated species. A 1-2˚C increase in SST may have profound effects on
biogeochemical cycles and the microbial loop as the microbial community is likely to
undergo shifts in abundance and composition that will affect the rates of cycling in
ways that we are not yet able to predict (Webster and Hill, 2007). For example,
increased SST may cause an increase in the abundance and activity of
bacterioplankton which would result in greater amounts of carbon passing through the
microbial loop and a concomitant reduction in carbon passing to higher trophic levels
(Webster and Hill, 2007). Consistent with this hypothesis was the reduced fish
production observed in response to a dominant microbial loop in the eastern
Mediterranean (Williams, 1998). Conversely, increased SST may cause a shift to a
less efficient bacterial community and a lower flux of carbon through the microbial
loop with potentially the opposite effect on fish populations. The important point is

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that the bacterial communities may be rapidly and significantly affected by small
shifts in temperature with potentially major flow-on consequences for other marine
organisms, because of the importance of bacterial communities in carbon flux through
the ecosystem.

If increased seawater temperature causes an increase in benthic bacterial productivity

there could be a corresponding increase in anaerobic processes as available oxygen is
rapidly utilised. Methanogenic archaea are present in anaerobic sediments so there is
also the potential for an increase in methanogenesis if anaerobic zones in sediments
are extended. This in turn, could increase the total production of methane, which
could be utilised by other microbes or fed back into the climate change cycle.
Anaerobic methane oxidation is a process of global importance in marine sediments
(Valentine, 2002) and is performed by at least two phylogenetically distinct groups of
archaea that are often observed in consortia with sulfate reducing bacteria.

The long-term burial of organic carbon in sediments results in the net accumulation of
oxygen in the atmosphere, thereby mediating climate change conditions (Weston and
Joye, 2005). Sediment microbial activity can play a fundamental role in determining
whether particulate organic carbon is recycled or buried. Temperature regulation of
the processes which lead to the microbial breakdown of complex particulate organic
carbon could therefore influence the rates of overall carbon mineralization. Currently
we have no knowledge on temperature effects for deep ocean carbon metabolism
despite the fact that this would probably have the largest influence on the global
carbon cycle. A study that examined carbon cycling in coastal anaerobic sediments
reported a variable temperature response of the key functional microbial groups that
mediate organic matter mineralization (Weston and Joye, 2005). In particular, the
Authors detected a greater temperature sensitivity of sulfate-reducing bacteria (whose
activity dominates the anaerobic terminal metabolic pathway in marine sediments)
than the temperature sensitivity of microbes involved in the hydrolysis /fermentation
of complex organic matter (Weston and Joye, 2005). This pioneering study showed
that microbial processes involved in organic carbon breakdown were extremely
sensitive to small changes in temperature, suggesting that global climate change may
significantly influence the efficiency of organic carbon recycling in coastal
ecosystems. Whilst these results pertain to a temperate system, it is conceivable that
microbes from a range of climes could respond in a similar way. However,
knowledge of microbial community composition and temperature thresholds for
individual species in sediments around Australia is currently too limited to predict the
response of key functional groups involved in organic carbon cycling.

It has recently been highlighted that climate change parameters such as elevated SSTs
may also have direct and indirect consequences on marine viruses, with potentially
cascading impacts on food webs, biogeochemical cycling, carbon sequestration and
the metabolic equilibrium of the ocean (Danovaro et al., 2011). Insufficient
knowledge of how marine viruses respond to temperature makes it difficult to predict
whether the viruses will exacerbate or attenuate the magnitude of climate change on
marine ecosystems. The abundance of marine viruses has been closely coupled to the
abundance of their hosts, so any change in the abundance, physiology or reproduction
of the prokaryotic host populations due to elevated SST will also affect viral
abundances (Danovaro et al., 2011). A greater understanding of temporal and spatial
trends in viral dynamics combined with better insights into host-virus dynamics in the

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Australian marine system are required so that marine virus components can be
included in future ocean climate models.

Microbial biofilms are well known to enhance settlement and metamorphosis in a

wide range of marine invertebrate species (reviewed by (Wieczorek and Todd, 1998)).
Increased SST may potentially cause changes in the composition of microbial
biofilms which could either alter the production of morphogenic signalling
compounds or affect the responses of larvae to these compounds. This would
obviously have a profound effect on patterns of larval settlement and subsequent
distribution of invertebrates and flow on implications for reef building, maintenance
and recovery processes. Limited knowledge of these processes and their probable
complexity makes it unlikely that these effects will be predictable. In one of the only
studies to test the thermal sensitivity of reef biofilms, the microbial community
associated with the crustose coralline algae Neogoniolithon fosliei was found to be
sensitive to temperatures of 32ºC (Webster et al., 2011b). In conjunction with the
microbial shift on CCA were clear indications of stress in the host CCA including
bleaching and a reduction in maximum quantum yield. A 50% reduction in the ability
of N. fosliei to induce coral larval metamorphosis at 32ºC accompanied the changes in
microbiology, pigmentation and photophysiology of the CCA. This research
demonstrates how thermal stress can influence microbial associations with subsequent
downstream impacts on coral recruitment which is critical for reef regeneration.

Dense microbial biofilms on

the surface of crustose coralline
algae (left, (Webster et al.,
2004)) provide settlement cues
for larvae of many coral
species (right, (Negri et al.,
2001)).

By virtue of their intimate and specific relationships, it is likely that microbial

symbionts have strict temperature thresholds. This is particularly important to marine
ecosystem health because a breakdown in symbiosis could result in host mortality,
reduced host fitness, shifts in hosts geographic range, increased disease or an increase
in predation/grazing. There is also the possibility that increased seawater temperatures
may cause a shift from a symbiotic to a pathogenic function for some microbial
species. Whilst the impact of elevated SSTs on marine symbioses has been well
studied for the coral-zooxanthellae relationship, there are comparatively few studies
exploring thermal sensitivity in other marine microbial symbioses.

In corals affected by temperature-induced bleaching, the microbial community shifts,

but then returns to normal once the environmental stress is removed (Bourne et al.,
2008). Interestingly, the coral-associated bacterial communities undergo changes prior
to any visible signs of stress (e.g. bleaching) in the coral host, indicating that the
microbial symbionts are a very sensitive indicator of stress. Functional shifts in coral

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microbial symbiosis have also been observed in the metagenomes of Porites

compressa exposed to a range of stressors including temperature (Vega Thurber et al.,
2008) and Acropora millepora during a natural bleaching event (Littman et al., 2011).
Both studies identified an increased abundance of microbial genes involved in
virulence and stress resistance along with significant changes in community
metabolism. These included shifts in secondary metabolism profiles, sulphur,
phosphorous and nitrogen metabolism, motility and chemotaxis, fatty acid and lipid
utilization pathways.

Some recent studies with sponges have also highlighted the effects of elevated
seawater temperatures on the symbiotic microbial associations (Lemoine et al., 2007;
López-Legentil et al., 2008; Webster et al., 2008; López-Legentil et al., 2010;
Webster et al., 2011a). These studies report shifts in the stable symbiotic microbial
communities that closely correlate with declines in sponge health. In the GBR sponge
Rhopaloeides odorabile, major changes in the symbiotic microbial community were
observed at 33°C. These included the loss of known sponge symbionts and the
appearance of a microbial community reflecting what is observed in diseased corals
(Webster et al., 2008). However, in contrast to the adult sponges, larval R. odorabile
exhibit a markedly higher thermal tolerance, with adverse health effects and a
concomittant microbial shift not occuring until 36°C (Webster et al., 2011a). These
sponge studies reveal distinct thermal tolerances in each of the life history stages and
confirm that at least 1 species of sponge larvae can maintain highly stable symbioses
at seawater temperatures exceeding those predicted under climate change. However,
these approaches must be interpreted with caution as temperature shift experiments
simply stress physiology whilst climate change which occurs gradually may select for
adaptation at the population level (based on genetic diversity).

Microbial diseases also have the potential to cause major impacts on population levels,
biodiversity and community structure of coral reef ecosystems by causing shifts in the
abundance of various groups. For example, disease outbreaks in the Caribbean have
caused unprecedented changes in reef ecosystems through the loss of key reef
organisms and coral cover (Aronson and Precht, 2001; Porter et al., 2001; Weil, 2004;
Weil et al., 2006). Within the GBR temperature stress is believed to be causing a
decline in coral cover and reef health (Willis et al., 2004; Bruno et al., 2007;
Sweatman et al., 2011) with an established link between coral disease outbreaks and
warm temperature anomalies at sites with high coral cover (Bruno et al., 2007).
Increasing SSTs are thought to be one of the primary factors in the global increase in
Vibrio-associated diseases (Harvell et al., 2002). For example, a recent study of
bacterioplankton in the North Sea correlated the long-term effects of ocean warming
on marine prokaryotic communities and observed an increased relative abundance of
Vibrio species (in particular Vibrio cholera) (Vezzulli et al., 2011). Climate-linked
mass mortality events of benthic invertebrates in the temperate north-western (NW)
Mediterranean Sea have also been reported (Cerrano et al., 2000; Linares et al., 2008;
Garrabou et al., 2009) and Vibrio infections have been identified as triggering some of
these disease outbreaks (Vezzuli et al., 2010; Vezzulli et al., 2011).

In the Gulf of Mexico, Dermo disease (caused by a protozoan parasite) which affects
the oyster Crassostrea virginica closely follows the ENSO cycle with prevalence and
infection intensity declining during El Niño events and rising during La Niña events
(Kim and Harvell, 2002). This relationship between Dermo epidemics and ENSO

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suggest that disease outbreaks may be able to be predicted by climatic models,

providing potential management strategies for oyster populations. Unfortunately, our
current disease epidemiology datasets for Australia (initiated for corals in 1998) are
not yet extensive enough for valid correlations to be made with the ENSO cycle.

Increasing SST may potentially alter the virulence mechanisms of pathogens as has
been seen with the coral pathogens Vibrio coralliilyticus and V. shiloi (Toren et al.,
1998; Banin et al., 2000; Banin et al., 2001; Banin et al., 2003; Ben-Haim et al., 2003;
Kimes et al., 2012). Vibrio coralliilyticus is an important pathogen of coral species
both within Australia and globally (Pollock et al., 2010). It was first described to
cause bleaching and tissue lysis in Pocillopora damicornis (Ben-Haim and
Rosenberg, 2002) and has recently been reported as the etiological agent for white
syndrome disease in the Pacific (Sussman et al., 2008). Pathogenicity of Vibrio
coralliilyticus has been shown to be temperature-dependent largely due to temperature
regulation of multiple virulence mechanisms. Virulence factors involved in motility,
host degradation, secretion, antimicrobial resistance and transcriptional regulation are
upregulated at the higher virulent temperature of 27Ԝ°C, concurrent with phenotypic
changes in motility, antibiotic resistance, hemolysis, cytotoxicity and
bioluminescence (Kimes et al., 2012).

Increasing SST may also have a more negative impact on the pathogen than on the
host (Lafferty, 1997), a situation that would facilitate recovery of infected populations.
It is also relevant to note that marine disease outbreaks appear to be caused by many
different types of pathogens – viruses, bacteria, fungi and parasites’, suggesting that
the increased incidence of disease observed with higher SSTs may be due to a
reduction in the health of the host organisms.

Despite the vulnerability of pelagic, benthic, symbiotic and pathogenic microbes to

temperature; diversity, rapid genetic turnover, functional redundancy, expression of
temperature regulated genes and lateral gene transfer could potentially infer some
resilience to the microbial ecosystem. Gene transfer is an important mechanism by
which microbes can interact in the environment and facilitates the exchange of DNA
which transforms other bacterial cells and enables populations to adapt or evolve.
Prokaryotes have several possibilities to transfer genes including transduction, where
genes are transferred by the activity of viruses. This causes the horizontal spread of
genes within a community and may contribute to diversity. In addition, the 'insurance
hypothesis' assumes that there are many species in an ecosystem, which can perform
the same or very similar functions (Yachi and Loreau, 1999). These redundant species
can take over ecosystem functions once a dominant species becomes extinct or
functionally obsolete. This insurance due to redundancy of species may result in a
resilience of ecosystem functions. However, to date there is very little direct evidence
of functional redundancy in the marine microbial ecosystem. In addition, the ‘rare
biosphere’ of bacteria recently identified by Sogin and coworkers (Sogin et al., 2006)
may provide some resilience to environmental change. It has been hypothesized that
this enormous diversity of low-abundance microbial populations could “explain how
microbial communities recover from environmental catastrophe” (Sogin et al., 2006).

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pH and aragonite saturation state

As with elevated SST, little is known about how marine microbial communities will
respond to changing ocean chemistry and the complexity of the communities make
any potential effects extremely difficult to predict. As stated in a recent review of
acidification and marine microbes: ‘All microbes have complex proton pumps that are
involved in bioenergetics, but it is not clear how microbes might respond to changes
in environmental proton balance’ (Joint et al., 2011). Until recently, the effect of pH
on microorganisms had primarily been assessed by observing growth and survival in a
few cultivated species. The responses of entire microbial communities, including
effects of pH on microbial processes requires much more research attention to be fully
elucidated.

Mesocosm experiments in Norway have shown a shift in the planktonic heterotrophic

microbial community in response to elevated CO2 although no effect on bacterial
abundance or activity occurred (Allgaier et al., 2008). In a separate mesocosm
experiment seawater was adjusted to pH 7.8 and subsequent nutrient addition initiated
a phytoplankton bloom which modified the pH by 0.3 pH units, bringing the seawater
back to present day levels in only 4 days (Gilbert et al., 2008). A recent investigation
that assessed pH effects on bacterial communities in the mucus, tissue and skeleton of
the coral A. eurystoma found distinctly different microbial communities at the lower
pH (Meron et al., 2011). This included an increased relative abundance of
Vibrionaceae and Alteromonadaceae (bacteria often associated with stressed and
diseased marine invertebrates) and an increase in overall antibacterial activity. Whilst
these findings indicate that pH may impact the coral-associated bacterial community,
the pH stress of 7.3 is extreme within current climate change scenarios. Another
recent study investigated the effects of ocean acidification on community composition
and microbial activity in Great Barrier Reef biofilms (Witt et al., 2011). Bacterial
community shifts were observed at elevated (~1140 ppm) pCO2 concentrations
including a decrease in the relative abundance of Alphaproteobacteria and an increase
in the relative abundance of Bacteroidetes. Elevated pCO2 also shifted the algal
communities within the biofilm, increasing the C and N content but having no effect
on O2 flux. This study of GBR biofilms indicates that bacterial biofilm communities
can rapidly adapt and reorganize in response to high pCO2.

Acidifying seawater can also cause an increase in the concentration of ammonium

ions and a decrease in the concentration of ammonia. Ammonia-oxidising
microorganisms are central to the nitrogen cycle and may be negatively affected if
they cannot oxidise the ammonium ions. This will have subsequent effects on the
denitrifying and nitrifying bacteria in the marine system (Webster and Hill, 2007).
Recent evidence indicates that marine nitrification rates are significantly reduced as
seawater becomes more acidic (Wickins, 1983; Ward, 1987; Furukawa et al., 1993;
Beman et al., 2011). The first comprehensive study of the effects of ocean
acidification on seawater nitrification rates was recently performed using seawater
collected from diverse oceanic sites – BATS, HOTS, Sargasso and SPOTS. pH
reduction ranged from 8.09 to 7.42 and in all cases, nitrification rates, as measured by
the oxidation of 15NH4+, were reduced, relative to controls, by between 8 to 38%
(Beman et al., 2011). The Author’s concluded that ocean acidification will have a
significant impact on nitrification globally. The large-scale inhibition of nitrification
and subsequent reduction of nitrite and nitrate concentrations could also result in a

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decrease in denitrification. This, in turn, could lead to the buildup of nitrogen and
unpredictable eutrophication phenomena (Webster and Hill, 2007).

When trying to predict the overall consequences of ocean acidification for microbial-
mediated biogeochemical processes, we need to consider that microbes in the present-
day ocean can experience large variations in pH. For example, phytoplankton blooms
can rapidly reduce pCO2, thereby increasing pH. Therefore marine microbes must be
capable of rapidly adapting to these changes in pH. In some marine environments,
microbes are already experiencing pH as low (or lower) than that predicted by IPCC
for 2100 (Joint et al., 2011). For example, microbial processes continue in regions
where respiration exceeds photosynthesis and where the decomposition of sinking
organic matter by aerobic respiration causes a release of CO2 and a concomitant
reduction in pH (such as the ocean station ALOHA in Hawaii where seawater below
350m already has a pH less than 7.8) (Joint et al., 2011).

Considering the importance of marine microbes in oceanic productivity, global cycles

and marine ecosystem health, future research is urgently required to determine if
marine microbial assemblages will continue to function at the lower pH values that
are projected for the near future and to determine whether microbes can acclimate to
the rapid rate of pH change currently being experienced in the ocean.

Sea- level rise

A rise of 0.1-0.9 m in sea level by 2100 could increase fluxes of nutrients and
pollutants entering the marine environment and have direct impacts upon microbial
communities as outlined below. In addition, a rising sea level may facilitate the
introduction of new microbes from terrestrial sources into the system. For example,
there is some thought that Aspergillus sydowii, a pathogen of sea fans that has caused
significant mortality in the Caribbean, originated in African dust samples (Weir et al.,
2004) and Bacillus thuriengensis used in insecticides has been associated with sponge
disease in Papua New Guinea (Cervino et al., 2006). However, there is still
considerable debate and confusion over the exact origin and etiological roles of these
putatively terrestrial pathogens.

Extreme events (cyclones, storms and floods)

More extreme weather events including cyclones, storms and floods could have major
effects on marine microbial communities. For example, predicted increases in cyclone
intensity in Northern Australian waters would impact on the marine microbial
populations due to resuspension of bottom sediments and associated carbon and
nutrients, directly affecting activity within the microbial loop. It is also foreseeable
that more extreme flood events would increase nutrient and contaminant runoff into
inshore systems potentially altering microbial community composition and function.
Increased nitrogen levels generally stimulate microbial growth and thereby influence
photosynthetic rates and carbon dioxide levels. An increased concentration of
nitrogen entering marine waters via river runoff would therefore have significant
implications for both micro and macro communities due to impacts on the microbial
loop, symbiotic relationships and disease processes.

The impacts of increased terrestrial inputs on microbes are extremely difficult to

predict or model because of the overwhelming complexity of marine microbial
communities. Bacterial activity can modify organic material even without large fluxes

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of organic material into bacteria (Azam, 1998). For example, the activity of slow-
growing bacteria on the surfaces of marine snow can produce large quantities of
ectohydrolase enzymes that efficiently solubilize the organic particulate matter,
releasing it into the surrounding water and reducing the sinking flux of carbon into
deep zones (Smith et al., 1992). A small shift in nutrient concentrations may change
the bacterial communities performing this activity and select for communities that are
either more of less efficient at this “uncoupled solubilization”, with resultant changes
in the flux of carbon through marine ecosystems even without marked changes in
bacterial numbers or activities. Similarly, some bacteria produce potent proteases that
result in higher rates of silica dissolution and less transport of silica into the deep
benthos, potentially resulting in higher diatom growth in the photic zone and greater
rates of photosynthesis. Once again, a small shift in the bacterial communities, to
favour bacteria with higher or lower rates of silica dissolution, could have profound
effects on carbon cycling (Bidle et al., 2002).

Nutrient enrichment may also increase the incidence and severity of marine epizootics,
as evidenced by an increase in the severity of coral disease in the Caribbean after
increased nutrient exposure (Bruno et al., 2003). Increases in the concentration of
inorganic nitrogen and phosphorous could affect disease dynamics by increasing
pathogen fitness and virulence (Kim and Harvell, 2002) or negatively impacting on
host immunity.

Ocean currents, circulation and mixed layer depth

Bacterioplankton were historically thought to be ubiquitous in the ocean (Dolan,
2005) and therefore largely unaffected by ocean currents and circulation. However,
there is accumulating evidence of microbial zonation in at least some open ocean
microbial populations. For example, microbial communities in Arctic seawater are
strongly influenced by oceanic circulation with archaeal communities that are
distinctly structured due to the temperature and salinity characteristics of the seawater
(Galand et al., 2009). The Author’s suggest that ‘shifting currents and water mass
boundaries resulting from climate change may well impact patterns of microbial
diversity by displacing whole biomes from their historic distributions. This relocation
could have the potential to establish a substantially different geography of microbial-
driven biogeochemical processes and associated oceanic production’. Despite the
importance of these findings, we currently have no data on the zonation of prokaryotic
communities within Australian waters.

Ultraviolet Light
Ultraviolet light is a powerful mutagen, interfering with DNA replication and
introducing errors during the cellular processes undertaken during DNA repair. A
study that examined the effects of UV exposure on natural Antarctic phytoplankton
and protozoans found that UV radiation altered the biomass and species composition
of the community (Davidson and Belbin, 2002). The changes to size and availability
of food to higher trophic levels could have major consequences by changing food web
structure and function and potentially influencing biogeochemical cycles. The
expected increases in UV radiation with climate change could potentially impact on
Australian microbial communities by increasing the rate of genetic change or causing
shifts in community composition with a decline in UV sensitive species and an
increased abundance of UV tolerant species. This could have significant implications
for the microbial loop and for pathogenic and symbiotic relationships. In addition UV

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exposure can cause viruses to change from a lysogenic to a lytic reproduction state.
The lytic cycle involves infection of the host, replication and release of viral progeny
from the lysed host cell. A switch to lytic viral replication may result in increased
bust cycles of marine bacterioplankton thereby altering biogeochemical cycling
parameters. However, as with the other climate change parameters addressed above,
empirical data for responses of the Australian marine microbial community to
increased UV exposure is lacking.

Key Points
 A lack of research effort into marine microbial communities makes the
prediction of global climate change impacts extremely difficult and fraught
with uncertainties.
 With the exception of a few targeted experimental studies of temperature and
acidification effects, there are no observed impacts of climate change on
microbial populations in Australia; primarily due to a lack of long-term
datasets.
 Considering the current knowledge of climate change impacts on microbial
communities globally, the two most important factors of climate change for
marine microbial populations are likely to be temperature and nutrient
enrichment.
 The reporting frequency of disease outbreaks affecting marine organisms is
increasing. Whether this is being driven by climate factors including increased
SST is still being debated. However, for some populations such as corals,
disease outbreaks have now been empirically linked with increased seawater
temperatures. With predicted higher temperatures in the future, microbial
mediated disease is likely to be a central factor in observed impacts.

Confidence Assessment: Observed Impacts

Marine microbial community abundance/community structure and function
There is LOW evidence and LOW consensus therefore LOW confidence of climate
driven impacts on marine microbial communities. This is because there is no evidence
yet in Australia due to a lack of long-term data sets and limited experimental testing.
Microbial Disease Impacts on Marine Systems
There is Medium evidence and LOW confidence of increased microbial-mediated
disease impacts in the marine ecosystem. This is because though disease is observed
the elucidation of causative agents is lacking in most cases and cannot yet be linked to
climate driven processes.

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Potential impacts by 2030 (and/or 2100)

Changes in community structure and function

There is LOW evidence from observed impacts elsewhere and LOW consensus in
those findings.
Microbial Disease Impacts on Marine Systems
There is MEDIUM evidence from observed impacts elsewhere and MEDIUM
consensus in those findings.
Acidification
There is LOW evidence from laboratory work and LOW consensus in those findings.
Nutrient enrichment
There is MEDIUM evidence from observed impacts elsewhere and models, and LOW
consensus in the nature of the responses.

Current and planned research effort and observations

As described above, there is an urgent need for research into how climate change will
affect marine microbial populations both in Australia and globally. A recent report
from the American Society of Microbiology (Reid, 2011) highlighted the need to
bridge the gap between microbiology and climate science using models. This report
also highlighted the need to develop a monitoring/data collection strategy, implement
validation processes to integrate data collection, modeling and experimentation and
further develop technologies such as remote sensing. Microbial systems in the
laboratory will provide an opportunity to do climate shift experiments that are
meaningful at the evolutionary level (unlike those that only test physiological
responses). These experiments will be possible using the National Sea Simulator
(SeaSim) currently under construction at the Australian Institute of Marine Science.
SeaSim will be a sophisticated research aquarium facility offering full control over
aquatic and atmospheric environments enabling short-term and sustained experiments
into global changes affecting factors such as temperature, ocean acidity, salinity,
sedimentation and contaminants. These kinds of experiments would complement
long-term data collection. In addition, analysis of seawater samples collected as part
of the IMOS initiative may provide valuable baseline data for observing climate
trends into the future.

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