FULL REPORT

Microbes









Lead Author: 

Nicole S. Webster 1

Co Authors: David G Bourne 1

Download this report in PDF format: Click here

What is happening?

The reporting frequency of microbialmediated disease outbreaks affecting marine organisms is increasing and could contain a climate change signal. Disease events (or breakdown in microbial symbioses) in corals, sponges and some other species have already been linked with warmer seawater temperatures.

What is expected?

With warmer temperatures in the future, microbial-mediated disease outbreaks or disruptions to symbiosis are likely to become more frequent and wide-spread.

What we are doing about it?

Initiatives are underway for monitoring long-term changes in microbial biodiversity through genomic analysis of water samples. Investigations of environmental stress thresholds for microbial symbioses of key marine species are also in progress. Construction of national infrastructure including the SEASim aquarium at AIMS and state-of-the-art facilities at SIMS will increase capacity to investigate changes in community structure and function of marine microorganisms under climate scenarios.

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.

Citation: 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). Retrieved from www.oceanclimatechange.org.au [Date]

Contact Details: 
1Australian Institute of Marine Science, PMB 3 Townsville, Queensland 4810, Australia
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Authors

Dr David Bourne

David-bourne-head-shot

Dr David Bourne is a Senior Research Scientist at the Australian Institute of Marine Science. He has extensive experience as a...
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Nicole Webster

Webster

Nicole Webster is a microbial ecologist at the Australian Institute of Marine Science where she works within the Marine Microbes and Symbiosis team....
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Scientific Review:

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 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 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 (top panel), tumours (middle panel) and brown band (bottom 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 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 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 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)).

 

Potential Impacts by the 2030s and 2100s: 


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 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 Great Barrier Reef (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 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 27 °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). 


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 GBR 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 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 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 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 sea surface temperature 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 Assessments

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.

Potential Impacts by the 2030s and 2100s: 


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.


Adaptation 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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