Background The Arctic and Antarctic are the two most geographically distant bioregions on earth. Recent sampling efforts and following metagenomics have shed light on the global ocean microbial diversity and function, yet the microbiota of polar regions has not been included in such global analyses. Results Here a metagenomic study of seawater samples (n = 60) collected from different depths at 28 locations in the Arctic and Antarctic zones was performed, together with metagenomes from the Tara Oceans. More than 7500 (19%) polar seawater-derived operational taxonomic units could not be identified in the Tara Oceans datasets, and more than 3,900,000 protein-coding gene orthologs had no hits in the Ocean Microbial Reference Gene Catalog. Analysis of 214 metagenome assembled genomes (MAGs) recovered from the polar seawater microbiomes, revealed strains that are prevalent in the polar regions while nearly undetectable in temperate seawater. Metabolic pathway reconstruction for these microbes suggested versatility for saccharide and lipids biosynthesis, nitrate and sulfate reduction, and CO2 fixation. Comparison between the Arctic and Antarctic microbiomes revealed that antibiotic resistance genes were enriched in the Arctic while functions like DNA recombination were enriched in the Antarctic. Conclusions Our data highlight the occurrence of dominant and locally enriched microbes in the Arctic and Antarctic seawater with unique functional traits for environmental adaption, and provide a foundation for analyzing the global ocean microbiome in a more complete perspective.
Culture enrichment was developed to discover the uncharted microbial species in the environmental microbiota. Yet this strategy has not been widely used to study microbes of deep-sea environments. Here, we report the cultivation and metagenomic analysis of oceanic sediment microbiota collected from 6,477 m deep in the Mariana Trench. The sediment samples were cultured anaerobically in the laboratory for 4 months, before being subjected to full-length 16S rRNA gene sequencing using the PacBio technique and metagenome sequencing using both the Illumina and Oxford Nanopore techniques. The 16S rRNA gene analyses revealed 437 operational taxonomic units specific to the cultured microbes, despite the lower diversity of the cultured microbiota in comparison with the original. Metagenome analyses revealed the prevalence of functions related to respiration, energy production, and stress response in the cultured microbes, suggesting these functions may contribute to microbial proliferation under laboratory conditions. Binning of the assembled metagenome contigs of the cultured microbiota generated four nearly complete genomes affiliated to yet unclassified species under the genera Alcanivorax, Idiomarina, Sulfitobacter, and Erythrobacter. Excepting Alcanivorax, the other three genera were almost undetectable in the original samples and largely enriched in the cultured samples. The four genomes possessed a variety of genes for carbohydrate utilization and nitrite reduction, pointing to an ability to respire diverse carbon sources using nitrite as the final electron acceptor. Taken together, the findings suggest that a combination of culture enrichment and long-read sequencing is an ideal way to mine novel microbial species in the hadal environment, particularly species that are rare in their native environmental niches, and thus expand our understanding of the hadal microbial diversity and function.
Thiosulfate oxidation by microbes has a major impact on global sulfur cycling. Here, we provide evidence that bacteria within various Roseobacter lineages are important for thiosulfate oxidation in marine biofilms. We isolate and sequence the genomes of 54 biofilm-associated Roseobacter strains, finding conserved sox gene clusters for thiosulfate oxidation and plasmids, pointing to a niche-specific lifestyle. Analysis of global ocean metagenomic data suggests that Roseobacter strains are abundant in biofilms and mats on various substrates, including stones, artificial surfaces, plant roots, and hydrothermal vent chimneys. Metatranscriptomic analysis indicates that the majority of active sox genes in biofilms belong to Roseobacter strains. Furthermore, we show that Roseobacter strains can grow and oxidize thiosulfate to sulfate under both aerobic and anaerobic conditions. Transcriptomic and membrane proteomic analyses of biofilms formed by a representative strain indicate that thiosulfate induces sox gene expression and alterations in cell membrane protein composition, and promotes biofilm formation and anaerobic respiration. We propose that bacteria of the Roseobacter group are major thiosulfate-oxidizers in marine biofilms, where anaerobic thiosulfate metabolism is preferred.
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