Krill body size drives particulate organic carbon export in West Antarctica.

The export of carbon from the ocean surface and storage in the ocean interior is important in the modulation of global climate1-4. The West Antarctic Peninsula experiences some of the largest summer particulate organic carbon (POC) export rates, and one of the fastest warming rates, in the world5,6. To understand how warming may alter carbon storage, it is necessary to first determine the patterns and ecological drivers of POC export7,8. Here we show that Antarctic krill (Euphausia superba) body size and life-history cycle, as opposed to their overall biomass or regional environmental factors, exert the dominant control on the POC flux. We measured POC fluxes over 21 years, the longest record in the Southern Ocean, and found a significant 5-year periodicity in the annual POC flux, which oscillated in synchrony with krill body size, peaking when the krill population was composed predominately of large individuals. Krill body size alters the POC flux through the production and export of size-varying faecal pellets9, which dominate the total flux. Decreases in winter sea ice10, an essential habitat for krill, are causing shifts in the krill population11, which may alter these export patterns of faecal pellets, leading to changes in ocean carbon storage.

Comparing temperature sensitivity of bacterial growth in Antarctic marine water and soil.

The western Antarctic Peninsula is an extreme low temperature environment that is warming rapidly due to global change. Little is known, however, on the temperature sensitivity of growth of microbial communities in Antarctic soils and in the surrounding oceanic waters. This is the first study that directly compares temperature adaptation of adjacent marine and terrestrial bacteria in a polar environment. The bacterial communities in the ocean were adapted to lower temperatures than those from nearby soil, with cardinal temperatures for growth in the ocean being the lowest so far reported for microbial communities. This was reflected in lower minimum (Tmin ) and optimum temperatures (Topt ) for growth in water (-17 and +20°C, respectively) than in soil (-11 and +27°C), with lower sensitivity to changes in temperature (Q10 ; 0-10°C interval) in Antarctic water (2.7) than in soil (3.9). This is likely due to the more stable low temperature conditions of Antarctic waters than soils, and the fact that maximum in situ temperatures in water are lower than in soils, at least in summer. Importantly, the thermally stable environment of Antarctic marine water makes it feasible to create a single temperature response curve for bacterial communities. This would thus allow for calculations of temperature-corrected growth rates, and thereby quantifying the influence of factors other than temperature on observed growth rates, as well as predicting the effects of future temperature increases on Antarctic marine bacteria.

Recurrent seascape units identify key ecological processes along the western Antarctic Peninsula.

The western Antarctic Peninsula (WAP) is a bellwether of global climate change and natural laboratory for identifying interactions between climate and ecosystems. The Palmer Long-Term Ecological Research (LTER) project has collected data on key ecological and environmental processes along the WAP since 1993. To better understand how key ecological parameters are changing across space and time, we developed a novel seascape classification approach based on in situ temperature, salinity, chlorophyll a, nitrate + nitrite, phosphate, and silicate. We anticipate that this approach will be broadly applicable to other geographical areas. Through the application of self-organizing maps (SOMs), we identified eight recurrent seascape units (SUs) in these data. These SUs have strong fidelity to known regional water masses but with an additional layer of biogeochemical detail, allowing us to identify multiple distinct nutrient profiles in several water masses. To identify the temporal and spatial distribution of these SUs, we mapped them across the Palmer LTER sampling grid via objective mapping of the original parameters. Analysis of the abundance and distribution of SUs since 1993 suggests two year types characterized by the partitioning of chlorophyll a into SUs with different spatial characteristics. By developing generalized linear models for correlated, time-lagged external drivers, we conclude that early spring sea ice conditions exert a strong influence on the distribution of chlorophyll a and nutrients along the WAP, but not necessarily the total chlorophyll a inventory. Because the distribution and density of phytoplankton biomass can have an impact on biomass transfer to the upper trophic levels, these results highlight anticipated links between the WAP marine ecosystem and climate.

Spring-summer net community production, new production, particle export and related water column biogeochemical processes in the marginal sea ice zone of the Western Antarctic Peninsula 2012-2014.

New production (New P, the rate of net primary production (NPP) supported by exogenously supplied limiting nutrients) and net community production (NCP, gross primary production not consumed by community respiration) are closely related but mechanistically distinct processes. They set the carbon balance in the upper ocean and define an upper limit for export from the system. The relationships, relative magnitudes and variability of New P (from 15NO3- uptake), O2 : argon-based NCP and sinking particle export (based on the 238U : 234Th disequilibrium) are increasingly well documented but still not clearly understood. This is especially true in remote regions such as polar marginal ice zones. Here we present a 3-year dataset of simultaneous measurements made at approximately 50 stations along the Western Antarctic Peninsula (WAP) continental shelf in midsummer (January) 2012-2014. Net seasonal-scale changes in water column inventories (0-150 m) of nitrate and iodide were also estimated at the same stations. The average daily rates based on inventory changes exceeded the shorter-term rate measurements. A major uncertainty in the relative magnitude of the inventory estimates is specifying the start of the growing season following sea-ice retreat. New P and NCP(O2) did not differ significantly. New P and NCP(O2) were significantly greater than sinking particle export from thorium-234. We suggest this is a persistent and systematic imbalance and that other processes such as vertical mixing and advection of suspended particles are important export pathways.This article is part of the theme issue 'The marine system of the west Antarctic Peninsula: status and strategy for progress in a region of rapid change'.

Inter-decadal variability of phytoplankton biomass along the coastal West Antarctic Peninsula.

The West Antarctic Peninsula (WAP) is a climatically sensitive region where periods of strong warming have caused significant changes in the marine ecosystem and food-web processes. Tight coupling between phytoplankton and higher trophic levels implies that the coastal WAP is a bottom-up controlled system, where changes in phytoplankton dynamics may largely impact other food-web components. Here, we analysed the inter-decadal time series of year-round chlorophyll-a (Chl) collected from three stations along the coastal WAP: Carlini Station at Potter Cove (PC) on King George Island, Palmer Station on Anvers Island and Rothera Station on Adelaide Island. There were trends towards increased phytoplankton biomass at Carlini Station (PC) and Palmer Station, while phytoplankton biomass declined significantly at Rothera Station over the studied period. The impacts of two relevant climate modes to the WAP, the El Niño-Southern Oscillation and the Southern Annular Mode, on winter and spring phytoplankton biomass appear to be different among the three sampling stations, suggesting an important role of local-scale forcing than large-scale forcing on phytoplankton dynamics at each station. The inter-annual variability of seasonal bloom progression derived from considering all three stations together captured ecologically meaningful, seasonally co-occurring bloom patterns which were primarily constrained by water-column stability strength. Our findings highlight a coupled link between phytoplankton and physical and climate dynamics along the coastal WAP, which may improve our understanding of overall WAP food-web responses to climate change and variability.This article is part of the theme issue 'The marine system of the West Antarctic Peninsula: status and strategy for progress in a region of rapid change'.

Marine bacteria exhibit a bipolar distribution.

The microbial cosmopolitan dispersion hypothesis often invoked to explain distribution patterns driven by high connectivity of oceanographic water masses and widespread dispersal ability has never been rigorously tested. By using a global marine bacterial dataset and iterative matrix randomization simulation, we show that marine bacteria exhibit a significantly greater dispersal limitation than predicted by our null model using the "everything is everywhere" tenet with no dispersal limitation scenario. Specifically, marine bacteria displayed bipolar distributions (i.e., species occurring exclusively at both poles and nowhere else) significantly less often than in the null model. Furthermore, we observed fewer taxa present in both hemispheres but more taxa present only in a single hemisphere than expected under the null model. Each of these trends diverged further from the null expectation as the compared habitats became more geographically distant but more environmentally similar. Our meta-analysis supported a latitudinal gradient in bacterial diversity with higher richness at lower latitudes, but decreased richness toward the poles. Bacteria in the tropics also demonstrated narrower latitudinal ranges at lower latitudes and relatively larger ranges in higher latitudes, conforming to the controversial macroecological pattern of the "Rapoport rule." Collectively, our findings suggest that bacteria follow biogeographic patterns more typical of macroscopic organisms, and that dispersal limitation, not just environmental selection, likely plays an important role. Distributions of microbes that deliver critical ecosystem services, particularly those in polar regions, may be vulnerable to the same impacts that environmental stressors, climate warming, and degradation in habitat quality are having on biodiversity in animal and plant species.

More, smaller bacteria in response to ocean's warming?

Heterotrophic bacteria play a major role in organic matter cycling in the ocean. Although the high abundances and relatively fast growth rates of coastal surface bacterioplankton make them suitable sentinels of global change, past analyses have largely overlooked this functional group. Here, time series analysis of a decade of monthly observations in temperate Atlantic coastal waters revealed strong seasonal patterns in the abundance, size and biomass of the ubiquitous flow-cytometric groups of low (LNA) and high nucleic acid (HNA) content bacteria. Over this relatively short period, we also found that bacterioplankton cells were significantly smaller, a trend that is consistent with the hypothesized temperature-driven decrease in body size. Although decadal cell shrinking was observed for both groups, it was only LNA cells that were strongly coherent, with ecological theories linking temperature, abundance and individual size on both the seasonal and interannual scale. We explain this finding because, relative to their HNA counterparts, marine LNA bacteria are less diverse, dominated by members of the SAR11 clade. Temperature manipulation experiments in 2012 confirmed a direct effect of warming on bacterial size. Concurrent with rising temperatures in spring, significant decadal trends of increasing standing stocks (3% per year) accompanied by decreasing mean cell size (-1% per year) suggest a major shift in community structure, with a larger contribution of LNA bacteria to total biomass. The increasing prevalence of these typically oligotrophic taxa may severely impact marine food webs and carbon fluxes by an overall decrease in the efficiency of the biological pump.

Climate change and Southern Ocean ecosystems I: how changes in physical habitats directly affect marine biota.

Antarctic and Southern Ocean (ASO) marine ecosystems have been changing for at least the last 30 years, including in response to increasing ocean temperatures and changes in the extent and seasonality of sea ice; the magnitude and direction of these changes differ between regions around Antarctica that could see populations of the same species changing differently in different regions. This article reviews current and expected changes in ASO physical habitats in response to climate change. It then reviews how these changes may impact the autecology of marine biota of this polar region: microbes, zooplankton, salps, Antarctic krill, fish, cephalopods, marine mammals, seabirds, and benthos. The general prognosis for ASO marine habitats is for an overall warming and freshening, strengthening of westerly winds, with a potential pole-ward movement of those winds and the frontal systems, and an increase in ocean eddy activity. Many habitat parameters will have regionally specific changes, particularly relating to sea ice characteristics and seasonal dynamics. Lower trophic levels are expected to move south as the ocean conditions in which they are currently found move pole-ward. For Antarctic krill and finfish, the latitudinal breadth of their range will depend on their tolerance of warming oceans and changes to productivity. Ocean acidification is a concern not only for calcifying organisms but also for crustaceans such as Antarctic krill; it is also likely to be the most important change in benthic habitats over the coming century. For marine mammals and birds, the expected changes primarily relate to their flexibility in moving to alternative locations for food and the energetic cost of longer or more complex foraging trips for those that are bound to breeding colonies. Few species are sufficiently well studied to make comprehensive species-specific vulnerability assessments possible. Priorities for future work are discussed.

Jellyfish blooms result in a major microbial respiratory sink of carbon in marine systems.

Jellyfish blooms occur in many estuarine and coastal regions and may be increasing in their magnitude and extent worldwide. Voracious jellyfish predation impacts food webs by converting large quantities of carbon (C), fixed by primary producers and consumed by secondary producers, into gelatinous biomass, which restricts C transfer to higher trophic levels because jellyfish are not readily consumed by other predators. In addition, jellyfish release colloidal and dissolved organic matter (jelly-DOM), and could further influence the functioning of coastal systems by altering microbial nutrient and DOM pathways, yet the links between jellyfish and bacterioplankton metabolism and community structure are unknown. Here we report that jellyfish released substantial quantities of extremely labile C-rich DOM, relative to nitrogen (25.6 ± 31.6 C:1N), which was quickly metabolized by bacterioplankton at uptake rates two to six times that of bulk DOM pools. When jelly-DOM was consumed it was shunted toward bacterial respiration rather than production, significantly reducing bacterial growth efficiencies by 10% to 15%. Jelly-DOM also favored the rapid growth and dominance of specific bacterial phylogenetic groups (primarily γ-proteobacteria) that were rare in ambient waters, implying that jelly-DOM was channeled through a small component of the in situ microbial assemblage and thus induced large changes in community composition. Our findings suggest major shifts in microbial structure and function associated with jellyfish blooms, and a large detour of C toward bacterial CO(2) production and away from higher trophic levels. These results further suggest fundamental transformations in the biogeochemical functioning and biological structure of food webs associated with jellyfish blooms.

Projected 21st-century changes in marine heterotrophic bacteria under climate change.

Marine heterotrophic Bacteria (or referred to as bacteria) play an important role in the ocean carbon cycle by utilizing, respiring, and remineralizing organic matter exported from the surface to deep ocean. Here, we investigate the responses of bacteria to climate change using a three-dimensional coupled ocean biogeochemical model with explicit bacterial dynamics as part of the Coupled Model Intercomparison Project Phase 6. First, we assess the credibility of the century-scale projections (2015-2099) of bacterial carbon stock and rates in the upper 100 m layer using skill scores and compilations of the measurements for the contemporary period (1988-2011). Second, we demonstrate that across different climate scenarios, the simulated bacterial biomass trends (2076-2099) are sensitive to the regional trends in temperature and organic carbon stocks. Bacterial carbon biomass declines by 5-10% globally, while it increases by 3-5% in the Southern Ocean where semi-labile dissolved organic carbon (DOC) stocks are relatively low and particle-attached bacteria dominate. While a full analysis of drivers underpinning the simulated changes in all bacterial stock and rates is not possible due to data constraints, we investigate the mechanisms of the changes in DOC uptake rates of free-living bacteria using the first-order Taylor decomposition. The results demonstrate that the increase in semi-labile DOC stocks drives the increase in DOC uptake rates in the Southern Ocean, while the increase in temperature drives the increase in DOC uptake rates in the northern high and low latitudes. Our study provides a systematic analysis of bacteria at global scale and a critical step toward a better understanding of how bacteria affect the functioning of the biological carbon pump and partitioning of organic carbon pools between surface and deep layers.

Depth drives the distribution of microbial ecological functions in the coastal western Antarctic Peninsula.

The Antarctic marine environment is a dynamic ecosystem where microorganisms play an important role in key biogeochemical cycles. Despite the role that microbes play in this ecosystem, little is known about the genetic and metabolic diversity of Antarctic marine microbes. In this study we leveraged DNA samples collected by the Palmer Long Term Ecological Research (LTER) project to sequence shotgun metagenomes of 48 key samples collected across the marine ecosystem of the western Antarctic Peninsula (wAP). We developed an in silico metagenomics pipeline (iMAGine) for processing metagenomic data and constructing metagenome-assembled genomes (MAGs), identifying a diverse genomic repertoire related to the carbon, sulfur, and nitrogen cycles. A novel analytical approach based on gene coverage was used to understand the differences in microbial community functions across depth and region. Our results showed that microbial community functions were partitioned based on depth. Bacterial members harbored diverse genes for carbohydrate transformation, indicating the availability of processes to convert complex carbons into simpler bioavailable forms. We generated 137 dereplicated MAGs giving us a new perspective on the role of prokaryotes in the coastal wAP. In particular, the presence of mixotrophic prokaryotes capable of autotrophic and heterotrophic lifestyles indicated a metabolically flexible community, which we hypothesize enables survival under rapidly changing conditions. Overall, the study identified key microbial community functions and created a valuable sequence library collection for future Antarctic genomics research.

Geographic and phylogenetic variation in bacterial biovolume as revealed by protein and nucleic acid staining.

Biovolume is an important characteristic of cells that shapes the contribution of microbes to total biomass and biogeochemical cycling. Most studies of bacterial cell volumes use DAPI (4',6'-diamidino-2-phenylindole), which stains nucleic acids and therefore only a portion of the cell. We used SYPRO Ruby protein stain combined with fluorescence in situ hybridization to examine biovolumes of bacteria in the total community, as well in phylogenetic subgroups. Protein-based volumes varied more and were consistently larger than DNA-based volumes by 3.3-fold on average. Bacterial cells were ca. 30% larger in the Arctic Ocean and Antarctic coastal waters than in temperate regimes. We hypothesized that geographic differences in the abundance of specific bacterial groups drove the observed patterns in biovolume. In support of this hypothesis, we found that Gammaproteobacteria and members of the Sphingobacteria-Flavobacteria group were larger in higher-latitude waters and that the mean volumes of both groups were larger than the mean bacterial volume in all environments tested. The mean cell size of SAR11 bacteria was larger than the mean cell size of the total bacterial community on average, although this varied. Protein staining increases the accuracy of biovolume measurements and gives insights into how the biomass of marine microbial communities varies over time and space.

Bacterial community segmentation facilitates the prediction of ecosystem function along the coast of the western Antarctic Peninsula.

Bacterial community structure can be combined with observations of ecophysiological data to build predictive models of microbial ecosystem function. These models are useful for understanding how function might change in response to a changing environment. Here we use five spring-summer seasons of bacterial community structure and flow cytometry data from a productive coastal site along the western Antarctic Peninsula to construct models of bacterial production (BP), an ecosystem function that heterotrophic bacteria provide. Through a novel application of emergent self-organizing maps we identified eight recurrent modes in the structure of the bacterial community. A model that combined bacterial abundance, mode and the fraction of cells belonging to the high nucleic acid population (fHNA; R2=0.730, P<0.001) best described BP. Abrupt transitions between modes during the 2013-2014 spring-summer season corresponded to rapid shifts in fHNA. We conclude that parameterizing community structure data via segmentation can yield useful insights into microbial ecosystem function and ecosystem processes.

Seasonal Shifts in Bacterial Community Responses to Phytoplankton-Derived Dissolved Organic Matter in the Western Antarctic Peninsula.

Bacterial consumption of dissolved organic matter (DOM) drives much of the movement of carbon through the oceanic food web and the global carbon cycle. Understanding complex interactions between bacteria and marine DOM remains an important challenge. We tested the hypothesis that bacterial growth and community succession would respond differently to DOM additions due to seasonal changes in phytoplankton abundance in the environment. Four mesocosm experiments were conducted that spanned the spring transitional period (August-December 2013) in surface waters of the Western Antarctic Peninsula (WAP). Each mesocosm consisted of nearshore surface seawater (50 L) incubated in the laboratory for 10 days. The addition of DOM, in the form of cell-free exudates extracted from Thalassiosira weissflogii diatom cultures led to changes in bacterial abundance, production, and community composition. The timing of each mesocosm experiment (i.e., late winter vs. late spring) influenced the magnitude and direction of bacterial changes. For example, the same DOM treatment applied at different times during the season resulted in different levels of bacterial production and different bacterial community composition. There was a mid-season shift from Collwelliaceae to Polaribacter having the greatest relative abundance after incubation. This shift corresponded to a modest but significant increase in the initial relative abundance of Polaribacter in the nearshore seawater used to set up experiments. This finding supports a new hypothesis that starting community composition, through priority effects, influenced the trajectory of community succession in response to DOM addition. As strong inter-annual variability and long-term climate change may shift the timing of WAP phytoplankton blooms, and the corresponding production of DOM exudates, this study suggests a mechanism by which different seasonal successional patterns in bacterial communities could occur.

Seasonal Succession of Free-Living Bacterial Communities in Coastal Waters of the Western Antarctic Peninsula.

The marine ecosystem along the Western Antarctic Peninsula undergoes a dramatic seasonal transition every spring, from almost total darkness to almost continuous sunlight, resulting in a cascade of environmental changes, including phytoplankton blooms that support a highly productive food web. Despite having important implications for the movement of energy and materials through this ecosystem, little is known about how these changes impact bacterial succession in this region. Using 16S rRNA gene amplicon sequencing, we measured changes in free-living bacterial community composition and richness during a 9-month period that spanned winter to the end of summer. Chlorophyll a concentrations were relatively low until summer when a major phytoplankton bloom occurred, followed 3 weeks later by a high peak in bacterial production. Richness in bacterial communities varied between ~1,200 and 1,800 observed operational taxonomic units (OTUs) before the major phytoplankton bloom (out of ~43,000 sequences per sample). During peak bacterial production, OTU richness decreased to ~700 OTUs. The significant decrease in OTU richness only lasted a few weeks, after which time OTU richness increased again as bacterial production declined toward pre-bloom levels. OTU richness was negatively correlated with bacterial production and chlorophyll a concentrations. Unlike the temporal pattern in OTU richness, community composition changed from winter to spring, prior to onset of the summer phytoplankton bloom. Community composition continued to change during the phytoplankton bloom, with increased relative abundance of several taxa associated with phytoplankton blooms, particularly Polaribacter. Bacterial community composition began to revert toward pre-bloom conditions as bacterial production declined. Overall, our findings clearly demonstrate the temporal relationship between phytoplankton blooms and seasonal succession in bacterial growth and community composition. Our study highlights the importance of high-resolution time series sampling, especially during the relatively under-sampled Antarctic winter and spring, which enabled us to discover seasonal changes in bacterial community composition that preceded the summertime phytoplankton bloom.

Seasonal time bombs: dominant temperate viruses affect Southern Ocean microbial dynamics.

Rapid warming in the highly productive western Antarctic Peninsula (WAP) region of the Southern Ocean has affected multiple trophic levels, yet viral influences on microbial processes and ecosystem function remain understudied in the Southern Ocean. Here we use cultivation-independent quantitative ecological and metagenomic assays, combined with new comparative bioinformatic techniques, to investigate double-stranded DNA viruses during the WAP spring-summer transition. This study demonstrates that (i) temperate viruses dominate this region, switching from lysogeny to lytic replication as bacterial production increases, and (ii) Southern Ocean viral assemblages are genetically distinct from lower-latitude assemblages, primarily driven by this temperate viral dominance. This new information suggests fundamentally different virus-host interactions in polar environments, where intense seasonal changes in bacterial production select for temperate viruses because of increased fitness imparted by the ability to switch replication strategies in response to resource availability. Further, temperate viral dominance may provide mechanisms (for example, bacterial mortality resulting from prophage induction) that help explain observed temporal delays between, and lower ratios of, bacterial and primary production in polar versus lower-latitude marine ecosystems. Together these results suggest that temperate virus-host interactions are critical to predicting changes in microbial dynamics brought on by warming in polar marine systems.

Microbial Communities Can Be Described by Metabolic Structure: A General Framework and Application to a Seasonally Variable, Depth-Stratified Microbial Community from the Coastal West Antarctic Peninsula.

Taxonomic marker gene studies, such as the 16S rRNA gene, have been used to successfully explore microbial diversity in a variety of marine, terrestrial, and host environments. For some of these environments long term sampling programs are beginning to build a historical record of microbial community structure. Although these 16S rRNA gene datasets do not intrinsically provide information on microbial metabolism or ecosystem function, this information can be developed by identifying metabolisms associated with related, phenotyped strains. Here we introduce the concept of metabolic inference; the systematic prediction of metabolism from phylogeny, and describe a complete pipeline for predicting the metabolic pathways likely to be found in a collection of 16S rRNA gene phylotypes. This framework includes a mechanism for assigning confidence to each metabolic inference that is based on a novel method for evaluating genomic plasticity. We applied this framework to 16S rRNA gene libraries from the West Antarctic Peninsula marine environment, including surface and deep summer samples and surface winter samples. Using statistical methods commonly applied to community ecology data we found that metabolic structure differed between summer surface and winter and deep samples, comparable to an analysis of community structure by 16S rRNA gene phylotypes. While taxonomic variance between samples was primarily driven by low abundance taxa, metabolic variance was attributable to both high and low abundance pathways. This suggests that clades with a high degree of functional redundancy can occupy distinct adjacent niches. Overall our findings demonstrate that inferred metabolism can be used in place of taxonomy to describe the structure of microbial communities. Coupling metabolic inference with targeted metagenomics and an improved collection of completed genomes could be a powerful way to analyze microbial communities in a high-throughput manner that provides direct access to metabolic and ecosystem function.