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Key Points The application of 'omic' approaches (for example, pyrosequencing, metagenomics, metatranscriptomics and metaproteomics) has generated unprecedented insight into Antarctic microorganisms and revealed intriguing properties about communities that can be linked to their Antarctic-specific habitats. Community composition and ecosystem function are controlled by the polar light regime, biotic and abiotic environmental factors, limnological history and seed populations, biogeography and the limits of aeolian and advective dispersal caused by physical barriers and distance between sites, and perturbation caused by ecosystem change. The polar austral summer is characterized by continuous high solar irradiance, which stimulates phototrophic growth and kinetically accelerates growth. Such communities tend to be oriented towards maximizing the effectiveness of light energy while switching to light-independent processes (for example, chemolithoautotrophy, phagotrophy and heterotrophic utilization of storage compounds) to survive the cold, dark winter. Virus–host interactions are particularly important in the Antarctic food web, in which they not only control remineralization and influence community composition but have unanticipated roles in influencing productivity cycles. Discoveries pertaining to viruses have included systems with a high diversity of novel eukaryotic viruses, phage-resistant bacteria, and archaea capable of evading, defending against and adapting to viruses. Unusual biogeochemical cycles have developed as a result of communities evolving in very specific, local environments. The indigenous communities have developed a range of traits, including a hierarchical structure, low complexity, niche adaptation, clonal dominance, mixotrophy and short-circuited nutrient cycles that enhance the use and conservation of resources. Specific taxa have a major influence on overall ecosystem function, with stability of those biomes being reliant on the key, specialized and fit members maintaining function and not being affected by ecosystem perturbation, particularly anthropocentric climate change and the introduction of alien species. Antarctica has an essential role in regulating Earth's climate and ocean ecosystem function, and Antarctica's biosphere is dominated by microorganisms. In this Review, Cavicchioli discusses the factors that shape the biogeography of Antarctic microorganisms and explores how 'omic' studies have begun to elucidate the mechanisms determining the composition and function of microbial communities in Antarctic aquatic systems. The Earth's biosphere is dominated by cold environments, and the cold biosphere is dominated by microorganisms. Microorganisms in cold Southern Ocean waters are recognized for having crucial roles in global biogeochemical cycles, including carbon sequestration, whereas microorganisms in other Antarctic aquatic biomes are not as well understood. In this Review, I consider what has been learned about Antarctic aquatic microbial ecology from 'omic' studies. I assess the factors that shape the biogeography of Antarctic microorganisms, reflect on some of the unusual biogeochemical cycles that they are associated with and discuss the important roles that viruses have in controlling ecosystem function.

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.

Although environmental selection and spatial separation have been shown to shape the distribution and abundance of marine microorganisms, the effects of advection (physical transport) have not been directly tested. Here we examine 25 samples covering all major water masses of the Southern Ocean to determine the effects of advection on microbial biogeography. Even when environmental factors and spatial separation are controlled for, there is a positive correlation between advection distance and taxonomic dissimilarity, indicating that an ‘advection effect’ has a role in shaping marine microbial community composition. This effect is likely due to the advection of cells increasing the probability that upstream microorganisms will colonize downstream sites. Our study shows that in addition to distance and environmental selection, advection shapes the composition of marine microbial communities. Environmental factors and distance are known to influence the structure of marine microbial communities. Using a data set spanning the Southern Ocean, Wilkins et al. now demonstrate that fluid transport (advection) is another important factor involved in shaping the marine microbial ecosystem.

Changes in the sequence of an organism’s genome, i.e., mutations, are the raw material of evolution. The frequency and location of mutations can be constrained by specific molecular mechanisms, such as diversity-generating retroelements (DGRs). DGRs have been characterized from cultivated bacteria and bacteriophages, and perform error-prone reverse transcription leading to mutations being introduced in specific target genes. DGR loci were also identified in several metagenomes, but the ecological roles and evolutionary drivers of these DGRs remain poorly understood. Here, we analyze a dataset of >30,000 DGRs from public metagenomes, establish six major lineages of DGRs including three primarily encoded by phages and seemingly used to diversify host attachment proteins, and demonstrate that DGRs are broadly active and responsible for >10% of all amino acid changes in some organisms. Overall, these results highlight the constraints under which DGRs evolve, and elucidate several distinct roles these elements play in natural communities. Here, the authors report a large-scale comparative analysis of <30,000 Diversity-Generating Retroelements (DGRs) across ~9000 metagenomes (representing diverse taxa and biomes), to identify patterns in terms of prevalence and activity. Combined with examination of longitudinal data on <100 metagenomes part of time series, they demonstrate that DGRs are broadly and consistently active, implying an important role in microbiota ecology and evolution.

Many marine bacteria have evolved to grow optimally at either high (copiotrophic) or low (oligotrophic) nutrient concentrations, enabling different species to colonize distinct trophic habitats in the oceans. Here, we compare the genome sequences of two bacteria, Photobacterium angustum S14 and Sphingopyxis alaskensis RB2256, that serve as useful model organisms for copiotrophic and oligotrophic modes of life and specifically relate the genomic features to trophic strategy for these organisms and define their molecular mechanisms of adaptation. We developed a model for predicting trophic lifestyle from genome sequence data and tested >400,000 proteins representing >500 million nucleotides of sequence data from 126 genome sequences with metagenome data of whole environmental samples. When applied to available oceanic metagenome data (e.g., the Global Ocean Survey data) the model demonstrated that oligotrophs, and not the more readily isolatable copiotrophs, dominate the ocean's free-living microbial populations. Using our model, it is now possible to define the types of bacteria that specific ocean niches are capable of sustaining.

Viruses are abundant ubiquitous members of microbial communities and in the marine environment affect population structure and nutrient cycling by infecting and lysing primary producers. Antarctic lakes are microbially dominated ecosystems supporting truncated food webs in which viruses exert a major influence on the microbial loop. Here we report the discovery of a virophage (relative of the recently described Sputnik virophage) that preys on phycodnaviruses that infect prasinophytes (phototrophic algae). By performing metaproteogenomic analysis on samples from Organic Lake, a hypersaline meromictic lake in Antarctica, complete virophage and near-complete phycodnavirus genomes were obtained. By introducing the virophage as an additional predator of a predator-prey dynamic model we determined that the virophage stimulates secondary production through the microbial loop by reducing overall mortality of the host and increasing the frequency of blooms during polar summer light periods. Virophages remained abundant in the lake 2 y later and were represented by populations with a. high level of major capsid protein sequence variation (25-100% identity). Virophage signatures were also found in neighboring Ace Lake (in abundance) and in two tropical lakes (hypersaline and fresh), an estuary, and an ocean upwelling site. These findings indicate that virophages regulate host-virus interactions, influence overall carbon flux in Organic Lake, and play previously unrecognized roles in diverse aquatic ecosystems.

The ubiquitous SAR11 bacterial clade is the most abundant type of organism in the world's oceans, but the reasons for its success are not fully elucidated. We analysed 128 surface marine metagenomes, including 37 new Antarctic metagenomes. The large size of the data set enabled internal transcribed spacer (ITS) regions to be obtained from the Southern polar region, enabling the first global characterization of the distribution of SAR11, from waters spanning temperatures −2 to 30°C. Our data show a stable co‐occurrence of phylotypes within both ‘tropical’ (>20°C) and ‘polar’ (<10°C) biomes, highlighting ecological niche differentiation between major SAR11 subgroups. All phylotypes display transitions in abundance that are strongly correlated with temperature and latitude. By assembling SAR11 genomes from Antarctic metagenome data, we identified specific genes, biases in gene functions and signatures of positive selection in the genomes of the polar SAR11—genomic signatures of adaptive radiation. Our data demonstrate the importance of adaptive radiation in the organism's ability to proliferate throughout the world's oceans, and describe genomic traits characteristic of different phylotypes in specific marine biomes. Metagenomic samples from oceans around the globe were used to examine the biogeography of the dominant marine heterotrophic bacterial clade, SAR11. Analysis uncovers evidence of adaptive radiation in response to environmental parameters, particularly temperature. Synopsis Metagenomic samples from oceans around the globe were used to examine the biogeography of the dominant marine heterotrophic bacterial clade, SAR11. Analysis uncovers evidence of adaptive radiation in response to environmental parameters, particularly temperature. By generating 37 new Antarctic metagenomes and analysing the internal transcribed spacer (ITS) regions of the SAR11 clade in a total of 128 surface marine metagenomes, we identified phylotype distributions that strongly correlated with temperature and latitude. By assembling SAR11 genomes from Antarctic metagenome data, we identified specific genes, biases in gene functions and signatures of positive selection in the genomes of the polar SAR11—genomic signatures of adaptive radiation. Our data demonstrate the importance of adaptive radiation in an organism's ability to proliferate throughout the world's oceans, and describe genomic traits characteristic of different phylotypes in specific marine biomes. These bacteria are important marine heterotrophs and have a fundamental role in oceanic nutrient cycling. These findings, therefore, have important implications for our ability to predict how changes in ocean temperature may affect bacterial ecology.

DPANN archaea are a diverse group of microorganisms characterised by small cells and reduced genomes. To date, all cultivated DPANN archaea are ectosymbionts that require direct cell contact with an archaeal host species for growth and survival. However, these interactions and their impact on the host species are poorly understood. Here, we show that a DPANN archaeon ( Candidatus Nanohaloarchaeum antarcticus) engages in parasitic interactions with its host ( Halorubrum lacusprofundi ) that result in host cell lysis. During these interactions, the nanohaloarchaeon appears to enter, or be engulfed by, the host cell. Our results provide experimental evidence for a predatory-like lifestyle of an archaeon, suggesting that at least some DPANN archaea may have roles in controlling host populations and their ecology. DPANN archaea are a group of microorganisms that require direct cell contact with other archaeal host species for growth. Here, Hamm et al. show that a DPANN archaeon engages in parasitic interactions with its host leading to host cell lysis, thus providing experimental evidence of a predatory-like lifestyle for an archaeon.

Key Points Studies of the Archaea have had a substantial impact on the field of biology. Carl Woese carried out several pioneering studies, examining the evolution of the genetic code, the translation apparatus and the cell as a whole, and the insight gained from his early work led to the discovery of the third domain. Defining moments in the history of archaeal research include the construction of a universal tree of life and the rationalization of the phylogeny of small-subunit ribosomal RNA, aminoacyl-tRNA synthetases and other protein sequences, leading to the three-domain view of life. Seminal advances were made through probing the biochemistry, physiology, genetics and evolution of methanogens, extreme halophiles and thermoacidophiles. The nature of archaea as extremophiles can now be placed into context with the knowledge that archaea are abundant and ubiquitous throughout the Earth's biosphere, including in the vast cold reaches of the planet. Archaea play a key part in maintaining important biogeochemical cycles, and several contemporary advances have been made in our understanding of the importance of archaea in global ecology. Technological advances have greatly enhanced the output from the field; particularly noteworthy are the impact of DNA sequencing, and the dawning of the genomics era and application of metagenomics, as well as breakthroughs that have been made through the development of tractable genetic systems. The Archaea evolved over 3 billion years ago but were only formally proposed as a domain 20 years ago. Today, many of the unique features and many of those that are shared with either the Bacteria or the Eukarya are well understood. Here, Ricardo Cavicchioli describes some of the important events in our appreciation of this fascinating group of organisms. The Archaea evolved as one of the three primary lineages several billion years ago, but the first archaea to be discovered were described in the scientific literature about 130 years ago. Moreover, the Archaea were formally proposed as the third domain of life only 20 years ago. Over this very short period of investigative history, the scientific community has learned many remarkable things about the Archaea — their unique cellular components and pathways, their abundance and critical function in diverse natural environments, and their quintessential role in shaping the evolutionary path of life on Earth. This Review charts the 'archaea movement', from its genesis through to key findings that, when viewed together, illustrate just how strongly the field has built on new knowledge to advance our understanding not only of the Archaea, but of biology as a whole.