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Background In Antarctica, summer sunlight enables phototrophic microorganisms to drive primary production, thereby “feeding” ecosystems to enable their persistence through the long, dark winter months. In Ace Lake, a stratified marine-derived system in the Vestfold Hills of East Antarctica, a Chlorobium species of green sulphur bacteria (GSB) is the dominant phototroph, although its seasonal abundance changes more than 100-fold. Here, we analysed 413 Gb of Antarctic metagenome data including 59 Chlorobium metagenome-assembled genomes (MAGs) from Ace Lake and nearby stratified marine basins to determine how genome variation and population structure across a 7-year period impacted ecosystem function. Results A single species, Candidatus Chlorobium antarcticum (most similar to Chlorobium phaeovibrioides DSM265) prevails in all three aquatic systems and harbours very little genomic variation (≥ 99% average nucleotide identity). A notable feature of variation that did exist related to the genomic capacity to biosynthesize cobalamin. The abundance of phylotypes with this capacity changed seasonally ~ 2-fold, consistent with the population balancing the value of a bolstered photosynthetic capacity in summer against an energetic cost in winter. The very high GSB concentration (> 108 cells ml−1 in Ace Lake) and seasonal cycle of cell lysis likely make Ca. Chlorobium antarcticum a major provider of cobalamin to the food web. Analysis of Ca. Chlorobium antarcticum viruses revealed the species to be infected by generalist (rather than specialist) viruses with a broad host range (e.g., infecting Gammaproteobacteria) that were present in diverse Antarctic lakes. The marked seasonal decrease in Ca. Chlorobium antarcticum abundance may restrict specialist viruses from establishing effective lifecycles, whereas generalist viruses may augment their proliferation using other hosts. Conclusion The factors shaping Antarctic microbial communities are gradually being defined. In addition to the cold, the annual variation in sunlight hours dictates which phototrophic species can grow and the extent to which they contribute to ecosystem processes. The Chlorobium population studied was inferred to provide cobalamin, in addition to carbon, nitrogen, hydrogen, and sulphur cycling, as critical ecosystem services. The specific Antarctic environmental factors and major ecosystem benefits afforded by this GSB likely explain why such a coherent population structure has developed in this Chlorobium species.

Diatoms, large bloom-forming marine microorganisms, build frustules out of silicate, which ballasts the cells and aids their export to the deep ocean. This unique physiology forges an important link between the marine silicon and carbon cycles. However, the effect of ocean acidification on the silicification of diatoms is unclear. Here we show that diatom silicification strongly diminishes with increased acidity in a natural Antarctic community. Analyses of single cells from within the community reveal that the effect of reduced pH on silicification differs among taxa, with several species having significantly reduced silica incorporation at CO2 levels equivalent to those projected for 2100. These findings suggest that, before the end of this century, ocean acidification may influence the carbon and silicon cycle by both altering the composition of the diatom assemblages and reducing cell ballasting, which will probably alter vertical flux of these elements to the deep ocean. Diatoms have silicate skeletons that affect their buoyancy in the ocean. Ocean acidification reduces silicification, with varying effects between species, and could alter the marine carbon and silica cycles through changes in community composition and sinking rates.

Primary production in the Southern Ocean is dominated by diatom-rich phytoplankton assemblages, whose individual physiological characteristics and community composition are strongly shaped by the environment, yet knowledge on how diatoms allocate cellular energy in response to ocean acidification (OA) is limited. Understanding such changes in allocation is integral to determining the nutritional quality of diatoms and the subsequent impacts on the trophic transfer of energy and nutrients. Using synchrotron-based Fourier transform infrared microspectroscopy, we analysed the macromolecular content of selected individual diatom taxa from a natural Antarctic phytoplankton community exposed to a gradient of fCO2 levels (288-1263 µatm). Strong species-specific differences in macromolecular partitioning were observed under OA. Large taxa showed preferential energy allocation towards proteins, while smaller taxa increased both lipid and protein stores at high fCO2 . If these changes are representative of future Antarctic diatom physiology, we may expect a shift away from lipid-rich large diatoms towards a community dominated by smaller taxa, but with higher lipid and protein stores than their present-day contemporaries, a response that could have cascading effects on food web dynamics in the Antarctic marine ecosystem.

Understanding the vulnerability of marine calcifiers to ocean acidification is a critical issue, especially in the Southern Ocean (SO), which is likely to be the one of the first, and most severely affected regions. Since the industrial revolution, ~30% of anthropogenic CO2 has been absorbed by the oceans. Seawater pH levels have already decreased by 0.1 and are predicted to decline by ~ 0.3 by the year 2100. This process, known as ocean acidification (OA), is shallowing the saturation horizon, which is the depth below which calcium carbonate (CaCO3) dissolves, likely increasing the vulnerability of many marine calcifiers to dissolution. The negative impact of OA may be seen first in species depositing more soluble CaCO3 mineral phases such as aragonite and high-Mg calcite (HMC). These negative effects may become even exacerbated by increasing sea temperatures. Here we combine a review and a quantitative meta-analysis to provide an overview of the current state of knowledge about skeletal mineralogy of major taxonomic groups of SO marine calcifiers and to make predictions about how OA might affect different taxa. We consider their geographic range, skeletal mineralogy, biological traits and potential strategies to overcome OA. The meta-analysis of studies investigating the effects of the OA on a range of biological responses such as shell state, development and growth rate shows response variation depending on mineralogical composition. Species-specific responses due to mineralogical composition suggest taxa with calcitic, aragonitic and HMC skeletons may be more vulnerable to the expected carbonate chemistry alterations, and low magnesium calcite (LMC) species may be mostly resilient. Environmental and biological control on the calcification process and/or Mg content in calcite, biological traits and physiological processes are also expected to influence species specific responses.

High-latitude oceans have been identified as particularly vulnerable to ocean acidification if anthropogenic CO2 emissions continue. Marine microbes are an essential part of the marine food web and are a critical link in biogeochemical processes in the ocean, such as the cycling of nutrients and carbon. Despite this, the response of Antarctic marine microbial communities to ocean acidification is poorly understood. We investigated the effect of increasing fCO2 on the growth of heterotrophic nanoflagellates (HNFs), nano- and picophytoplankton, and prokaryotes (heterotrophic Bacteria and Archaea) in a natural coastal Antarctic marine microbial community from Prydz Bay, East Antarctica. At CO2 levels ≥634 µatm, HNF abundance was reduced, coinciding with increased abundance of picophytoplankton and prokaryotes. This increase in picophytoplankton and prokaryote abundance was likely due to a reduction in top-down control of grazing HNFs. Nanophytoplankton abundance was elevated in the 634 µatm treatment, suggesting that moderate increases in CO2 may stimulate growth. The taxonomic and morphological differences in CO2 tolerance we observed are likely to favour dominance of microbial communities by prokaryotes, nanophytoplankton, and picophytoplankton. Such changes in predator–prey interactions with ocean acidification could have a significant effect on the food web and biogeochemistry in the Southern Ocean, intensifying organic-matter recycling in surface waters; reducing vertical carbon flux; and reducing the quality, quantity, and availability of food for higher trophic levels.

Significance We demonstrate that Candidatus Nanohaloarchaeum antarcticus requires Halorubrum lacusprofundi for growth, illustrating that Nanohaloarchaeota require a host rather than being free living as previously proposed. Developing the means of cultivating Nanohaloarchaeota in the laboratory provides the capacity to advance understanding of how archaea interact and the factors that control their symbiotic relationship (e.g. mutualism, commensalism, antagonism). Our findings amplify the view that Antarctic lakes are a treasure trove for the discovery of microbes with previously unknown properties., In hypersaline environments, Nanohaloarchaeota (Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota, Nanohaloarchaeota [DPANN] superphylum) are thought to be free-living microorganisms. We report cultivation of 2 strains of Antarctic Nanohaloarchaeota and show that they require the haloarchaeon Halorubrum lacusprofundi for growth. By performing growth using enrichments and fluorescence-activated cell sorting, we demonstrated successful cultivation of Candidatus Nanohaloarchaeum antarcticus, purification of Ca. Nha. antarcticus away from other species, and growth and verification of Ca. Nha. antarcticus with Hrr. lacusprofundi; these findings are analogous to those required for fulfilling Koch’s postulates. We use fluorescent in situ hybridization and transmission electron microscopy to assess cell structures and interactions; metagenomics to characterize enrichment taxa, generate metagenome assembled genomes, and interrogate Antarctic communities; and proteomics to assess metabolic pathways and speculate about the roles of certain proteins. Metagenome analysis indicates the presence of a single species, which is endemic to Antarctic hypersaline systems that support the growth of haloarchaea. The presence of unusually large proteins predicted to function in attachment and invasion of hosts plus the absence of key biosynthetic pathways (e.g., lipids) in metagenome assembled genomes of globally distributed Nanohaloarchaeota indicate that all members of the lineage have evolved as symbionts. Our work expands the range of archaeal symbiotic lifestyles and provides a genetically tractable model system for advancing understanding of the factors controlling microbial symbiotic relationships.

Background The genomes of halophilic archaea (haloarchaea) often comprise multiple replicons. Genomic variation in haloarchaea has been linked to viral infection pressure and, in the case of Antarctic communities, can be caused by intergenera gene exchange. To expand understanding of genome variation and biogeography of Antarctic haloarchaea, here we assessed genomic variation between two strains of Halorubrum lacusprofundi that were isolated from Antarctic hypersaline lakes from different regions (Vestfold Hills and Rauer Islands). To assess variation in haloarchaeal populations, including the presence of genomic islands, metagenomes from six hypersaline Antarctic lakes were characterised. Results The sequence of the largest replicon of each Hrr. lacusprofundi strain (primary replicon) was highly conserved, while each of the strains’ two smaller replicons (secondary replicons) were highly variable. Intergenera gene exchange was identified, including the sharing of a type I-B CRISPR system. Evaluation of infectivity of an Antarctic halovirus provided experimental evidence for the differential susceptibility of the strains, bolstering inferences that strain variation is important for modulating interactions with viruses. A relationship was found between genomic structuring and the location of variation within replicons and genomic islands, demonstrating that the way in which haloarchaea accommodate genomic variability relates to replicon structuring. Metagenome read and contig mapping and clustering and scaling analyses demonstrated biogeographical patterning of variation consistent with environment and distance effects. The metagenome data also demonstrated that specific haloarchaeal species dominated the hypersaline systems indicating they are endemic to Antarctica. Conclusion The study describes how genomic variation manifests in Antarctic-lake haloarchaeal communities and provides the basis for future assessments of Antarctic regional and global biogeography of haloarchaea. Electronic supplementary material The online version of this article (10.1186/s40168-018-0495-3) contains supplementary material, which is available to authorized users.