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ItemInsights into the Vertical Stratification of Microbial Ecological Roles across the Deepest Seawater Column on Earth.(MDPI AG, 2020-08-27)The Earth's oceans are a huge body of water with physicochemical properties and microbial community profiles that change with depth, which in turn influences their biogeochemical cycling potential. The differences between microbial communities and their functional potential in surface to hadopelagic water samples are only beginning to be explored. Here, we used metagenomics to investigate the microbial communities and their potential to drive biogeochemical cycling in seven different water layers down the vertical profile of the Challenger Deep (0-10,500 m) in the Mariana Trench, the deepest natural point in the Earth's oceans. We recovered 726 metagenome-assembled genomes (MAGs) affiliated to 27 phyla. Overall, biodiversity increased in line with increased depth. In addition, the genome size of MAGs at ≥4000 m layers was slightly larger compared to those at 0-2000 m. As expected, surface waters were the main source of primary production, predominantly from Cyanobacteria. Intriguingly, microbes conducting an unusual form of nitrogen metabolism were identified in the deepest waters (>10,000 m), as demonstrated by an enrichment of genes encoding proteins involved in dissimilatory nitrate to ammonia conversion (DNRA), nitrogen fixation and urea transport. These likely facilitate the survival of ammonia-oxidizing archaea α lineage, which are typically present in environments with a high ammonia concentration. In addition, the microbial potential for oxidative phosphorylation and the glyoxylate shunt was enhanced in >10,000 m waters. This study provides novel insights into how microbial communities and their genetic potential for biogeochemical cycling differs through the Challenger deep water column, and into the unique adaptive lifestyle of microbes in the Earth's deepest seawater.
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ItemAncestral niche separation and evolutionary rate differentiation between sister marine flavobacteria lineages(WILEY, 2020-08)Marine flavobacteria are specialists for polysaccharide degradation. They dominate in habitats enriched with polysaccharides, but are also prevalent in pelagic environments where polysaccharides are less available. These niches are likely occupied by distinct lineages, but evolutionary processes underlying their niche differentiation remain elusive. Here, genomic analyses and physiological assays indicate that the sister flavobacteria lineages Leeuwenhoekiella and Nonlabens likely explore polysaccharide-rich macroalgae and polysaccharide-poor pelagic niches respectively. Phylogenomic analyses inferred that the niche separation likely occurred anciently and coincided with increased sequence evolutionary rate in Nonlabens compared with Leeuwenhoekiella. Further analyses ruled out the known mechanisms likely driving evolutionary rate acceleration, including reduced selection efficiency, decreased generation time and increased mutation rate. In particular, the mutation rates were determined using an unbiased experimental method, which measures the present-day populations and may not reflect ancestral populations. These data collectively lead to a new hypothesis that an ancestral and transient mutation rate increase resulted in evolutionary rate increase in Nonlabens. This hypothesis was supported by inferring that gains and losses of genes involved in SOS response, a mechanism known to drive transiently increased mutation rate, coincided with evolutionary rate acceleration. Our analyses highlight the evolutionary mechanisms underlying niche differentiation of flavobacteria lineages.
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ItemNovel insights into the Thaumarchaeota in the deepest oceans: their metabolism and potential adaptation mechanisms(BMC, 2020-06-01)BACKGROUND: Marine Group I (MGI) Thaumarchaeota, which play key roles in the global biogeochemical cycling of nitrogen and carbon (ammonia oxidizers), thrive in the aphotic deep sea with massive populations. Recent studies have revealed that MGI Thaumarchaeota were present in the deepest part of oceans-the hadal zone (depth > 6000 m, consisting almost entirely of trenches), with the predominant phylotype being distinct from that in the "shallower" deep sea. However, little is known about the metabolism and distribution of these ammonia oxidizers in the hadal water. RESULTS: In this study, metagenomic data were obtained from 0-10,500 m deep seawater samples from the Mariana Trench. The distribution patterns of Thaumarchaeota derived from metagenomics and 16S rRNA gene sequencing were in line with that reported in previous studies: abundance of Thaumarchaeota peaked in bathypelagic zone (depth 1000-4000 m) and the predominant clade shifted in the hadal zone. Several metagenome-assembled thaumarchaeotal genomes were recovered, including a near-complete one representing the dominant hadal phylotype of MGI. Using comparative genomics, we predict that unexpected genes involved in bioenergetics, including two distinct ATP synthase genes (predicted to be coupled with H+ and Na+ respectively), and genes horizontally transferred from other extremophiles, such as those encoding putative di-myo-inositol-phosphate (DIP) synthases, might significantly contribute to the success of this hadal clade under the extreme condition. We also found that hadal MGI have the genetic potential to import a far higher range of organic compounds than their shallower water counterparts. Despite this trait, hadal MDI ammonia oxidation and carbon fixation genes are highly transcribed providing evidence they are likely autotrophic, contributing to the primary production in the aphotic deep sea. CONCLUSIONS: Our study reveals potentially novel adaptation mechanisms of deep-sea thaumarchaeotal clades and suggests key functions of deep-sea Thaumarchaeota in carbon and nitrogen cycling. Video Abstract.