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.

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.

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.

Dynamic trophic shifts in bacterial and eukaryotic communities during the first 30 years of microbial succession following retreat of an Antarctic glacier.

We examined microbial succession along a glacier forefront in the Antarctic Peninsula representing ∼30 years of deglaciation to contrast bacterial and eukaryotic successional dynamics and abiotic drivers of community assembly using sequencing and soil properties. Microbial communities changed most rapidly early along the chronosequence, and co-occurrence network analysis showed the most complex topology at the earliest stage. Initial microbial communities were dominated by microorganisms derived from the glacial environment, whereas later stages hosted a mixed community of taxa associated with soils. Eukaryotes became increasingly dominated by Cercozoa, particularly Vampyrellidae, indicating a previously unappreciated role for cercozoan predators during early stages of primary succession. Chlorophytes and Charophytes (rather than cyanobacteria) were the dominant primary producers and there was a spatio-temporal sequence in which major groups became abundant succeeding from simple ice Chlorophytes to Ochrophytes and Bryophytes. Time since deglaciation and pH were the main abiotic drivers structuring both bacterial and eukaryotic communities. Determinism was the dominant assembly mechanism for Bacteria, while the balance between stochastic/deterministic processes in eukaryotes varied along the distance from the glacier front. This study provides new insights into the unexpected dynamic changes and interactions across multiple trophic groups during primary succession in a rapidly changing polar ecosystem.

Decline in plankton diversity and carbon flux with reduced sea ice extent along the Western Antarctic Peninsula.

Since the middle of the past century, the Western Antarctic Peninsula has warmed rapidly with a significant loss of sea ice but the impacts on plankton biodiversity and carbon cycling remain an open question. Here, using a 5-year dataset of eukaryotic plankton DNA metabarcoding, we assess changes in biodiversity and net community production in this region. Our results show that sea-ice extent is a dominant factor influencing eukaryotic plankton community composition, biodiversity, and net community production. Species richness and evenness decline with an increase in sea surface temperature (SST). In regions with low SST and shallow mixed layers, the community was dominated by a diverse assemblage of diatoms and dinoflagellates. Conversely, less diverse plankton assemblages were observed in waters with higher SST and/or deep mixed layers when sea ice extent was lower. A genetic programming machine-learning model explained up to 80% of the net community production variability at the Western Antarctic Peninsula. Among the biological explanatory variables, the sea-ice environment associated plankton assemblage is the best predictor of net community production. We conclude that eukaryotic plankton diversity and carbon cycling at the Western Antarctic Peninsula are strongly linked to sea-ice conditions.

Water quality measurements in Buzzards Bay by the Buzzards Bay Coalition Baywatchers Program from 1992 to 2018.

The Buzzards Bay Coalition's Baywatchers Monitoring Program (Baywatchers) collected summertime water quality information at more than 150 stations around Buzzards Bay, Massachusetts from 1992 to 2018. Baywatchers documents nutrient-related water quality and the effects of nitrogen pollution. The large majority of stations are located in sub-estuaries of the main Bay, although stations in central Buzzards Bay and Vineyard Sound were added beginning in 2007. Measurements include temperature, salinity, Secchi depth and concentrations of dissolved oxygen, ammonium, nitrate + nitrite, total dissolved nitrogen, particulate organic nitrogen, particulate organic carbon, ortho-phosphate, chlorophyll a, pheophytin a, and in lower salinity waters, total phosphorus and dissolved organic carbon. The Baywatchers dataset provides a long-term record of the water quality of Buzzards Bay and its sub-estuaries. The data have been used to identify impaired waters, evaluate discharge permits, support the development of nitrogen total maximum daily loads, develop strategies for reducing nitrogen inputs, and increase public awareness and generate support for management actions to control nutrient pollution and improve water quality.

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.

Global sea-surface iodide observations, 1967-2018.

The marine iodine cycle has significant impacts on air quality and atmospheric chemistry. Specifically, the reaction of iodide with ozone in the top few micrometres of the surface ocean is an important sink for tropospheric ozone (a pollutant gas) and the dominant source of reactive iodine to the atmosphere. Sea surface iodide parameterisations are now being implemented in air quality models, but these are currently a major source of uncertainty. Relatively little observational data is available to estimate the global surface iodide concentrations, and this data has not hitherto been openly available in a collated, digital form. Here we present all available sea surface (<20 m depth) iodide observations. The dataset includes values digitised from published manuscripts, published and unpublished data supplied directly by the originators, and data obtained from repositories. It contains 1342 data points, and spans latitudes from 70°S to 68°N, representing all major basins. The data may be used to model sea surface iodide concentrations or as a reference for future observations.

Towards Quantitative Microbiome Community Profiling Using Internal Standards.

An inherent issue in high-throughput rRNA gene tag sequencing microbiome surveys is that they provide compositional data in relative abundances. This often leads to spurious correlations, making the interpretation of relationships to biogeochemical rates challenging. To overcome this issue, we quantitatively estimated the abundance of microorganisms by spiking in known amounts of internal DNA standards. Using a 3-year sample set of diverse microbial communities from the Western Antarctica Peninsula, we demonstrated that the internal standard method yielded community profiles and taxon cooccurrence patterns substantially different from those derived using relative abundances. We found that the method provided results consistent with the traditional CHEMTAX analysis of pigments and total bacterial counts by flow cytometry. Using the internal standard method, we also showed that chloroplast 16S rRNA gene data in microbial surveys can be used to estimate abundances of certain eukaryotic phototrophs such as cryptophytes and diatoms. In Phaeocystis, scatter in the 16S/18S rRNA gene ratio may be explained by physiological adaptation to environmental conditions. We conclude that the internal standard method, when applied to rRNA gene microbial community profiling, is quantitative and that its application will substantially improve our understanding of microbial ecosystems.IMPORTANCE High-throughput-sequencing-based marine microbiome profiling is rapidly expanding and changing how we study the oceans. Although powerful, the technique is not fully quantitative; it provides taxon counts only in relative abundances. In order to address this issue, we present a method to quantitatively estimate microbial abundances per unit volume of seawater filtered by spiking known amounts of internal DNA standards into each sample. We validated this method by comparing the calculated abundances to other independent estimates, including chemical markers (pigments) and total bacterial cell counts by flow cytometry. The internal standard approach allows us to quantitatively estimate and compare marine microbial community profiles, with important implications for linking environmental microbiomes to quantitative processes such as metabolic and biogeochemical rates.

Changes in the upper ocean mixed layer and phytoplankton productivity along the West Antarctic Peninsula.

The West Antarctic Peninsula (WAP) has experienced significant change over the last 50 years. Using a 24 year spatial time series collected by the Palmer Long Term Ecological Research programme, we assessed long-term patterns in the sea ice, upper mixed layer depth (MLD) and phytoplankton productivity. The number of sea ice days steadily declined from the 1980s until a recent reversal that began in 2008. Results show regional differences between the northern and southern regions sampled during regional ship surveys conducted each austral summer. In the southern WAP, upper ocean MLD has shallowed by a factor of 2. Associated with the shallower mixed layer is enhanced phytoplankton carbon fixation. In the north, significant interannual variability resulted in the mixed layer showing no trended change over time and there was no significant increase in the phytoplankton productivity. Associated with the recent increases in sea ice there has been an increase in the photosynthetic efficiency (chlorophyll a-normalized carbon fixation) in the northern and southern regions of the WAP. We hypothesize the increase in sea ice results in increased micronutrient delivery to the continental shelf which in turn leads to enhanced photosynthetic performance.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'.

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'.

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.

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.

Specific eukaryotic plankton are good predictors of net community production in the Western Antarctic Peninsula.

Despite our current realization of the tremendous diversity that exists in plankton communities, we have little understanding of how this biodiversity influences the biological carbon pump other than broad paradigms such as diatoms contributing disproportionally to carbon export. Here we combine high-resolution underway O2/Ar, which provides an estimate of net community production, with high-throughput 18 S ribosomal DNA sequencing to elucidate the relationship between eukaryotic plankton community structure and carbon export potential at the Western Antarctica Peninsula (WAP), a region which has experienced rapid warming and ecosystem changes. Our results show that in a diverse plankton system comprised of ~464 operational taxonomic units (OTUs) with at least 97% 18 S identity, as few as two or three key OTUs, i.e. large diatoms, Phaeocystis, and mixotrophic/phagotrophic dinoflagellates, can explain a large majority of the spatial variability in the carbon export potential (76-92%). Moreover, we find based on a community co-occurrence network analysis that ecosystems with lower export potential have more tightly coupled communities. Our results indicate that defining plankton communities at a deeper taxonomic resolution than by functional groups and accounting for the differences in size and coupling between groups can substantially improve organic carbon flux predictions.

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.