Metabolic potential and in situ transcriptomic profiles of previously uncharacterized key microbial groups involved in coupled carbon, nitrogen and sulfur cycling in anoxic marine zones (original) (raw)
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Genomic properties of Marine Group A bacteria indicate a role in the marine sulfur cycle
The ISME Journal, 2014
Marine Group A (MGA) is a deeply branching and uncultivated phylum of bacteria. Although their functional roles remain elusive, MGA subgroups are particularly abundant and diverse in oxygen minimum zones and permanent or seasonally stratified anoxic basins, suggesting metabolic adaptation to oxygen-deficiency. Here, we expand a previous survey of MGA diversity in O 2 -deficient waters of the Northeast subarctic Pacific Ocean (NESAP) to include Saanich Inlet (SI), an anoxic fjord with seasonal O 2 gradients and periodic sulfide accumulation. Phylogenetic analysis of small subunit ribosomal RNA (16S rRNA) gene clone libraries recovered five previously described MGA subgroups and defined three novel subgroups (SHBH1141, SHBH391, and SHAN400) in SI. To discern the functional properties of MGA residing along gradients of O 2 in the NESAP and SI, we identified and sequenced to completion 14 fosmids harboring MGA-associated 16S RNA genes from a collection of 46 fosmid libraries sourced from NESAP and SI waters. Comparative analysis of these fosmids, in addition to four publicly available MGA-associated large-insert DNA fragments from Hawaii Ocean Time-series and Monterey Bay, revealed widespread genomic differentiation proximal to the ribosomal RNA operon that did not consistently reflect subgroup partitioning patterns observed in 16S rRNA gene clone libraries. Predicted protein-coding genes associated with adaptation to O 2 -deficiency and sulfur-based energy metabolism were detected on multiple fosmids, including polysulfide reductase (psrABC), implicated in dissimilatory polysulfide reduction to hydrogen sulfide and dissimilatory sulfur oxidation. These results posit a potential role for specific MGA subgroups in the marine sulfur cycle.
2019
Proteobacteria constitute the most diverse and abundant group of microbes on Earth. In productive marine environments like deep-sea hydrothermal systems, Proteobacteria have been implicated in autotrophy coupled to sulfur, methane, and hydrogen oxidation, sulfate reduction, and denitrification. Beyond chemoautotrophy, little is known about the ecological significance of novel Proteobacteria that are globally distributed and active in hydrothermal systems. Here we apply multi-omics to characterize 51 metagenome-assembled genomes from three hydrothermal vent plumes in the Pacific and Atlantic Oceans that are affiliated with nine novel Proteobacteria lineages. Metabolic analyses revealed these organisms to contain a diverse functional repertoire including chemolithotrophic ability to utilize sulfur and C1compounds, and chemoorganotrophic ability to utilize environment-derived fatty acids, aromatics, carbohydrates, and peptides. Comparative genomics with marine and terrestrial microbiom...
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PLoS ONE, 2014
Ammonia-oxidizing archaea (AOA) are ubiquitous and abundant and contribute significantly to the carbon and nitrogen cycles in the ocean. In this study, we assembled AOA draft genomes from two deep marine sediments from Donghae, South Korea, and Svalbard, Arctic region, by sequencing the enriched metagenomes. Three major microorganism clusters belonging to Thaumarchaeota, Epsilonproteobacteria, and Gammaproteobacteria were deduced from their 16S rRNA genes, GC contents, and oligonucleotide frequencies. Three archaeal genomes were identified, two of which were distinct and were designated Ca. ''Nitrosopumilus koreensis'' AR1 and ''Nitrosopumilus sediminis'' AR2. AR1 and AR2 exhibited average nucleotide identities of 85.2% and 79.5% to N. maritimus, respectively. The AR1 and AR2 genomes contained genes pertaining to energy metabolism and carbon fixation as conserved in other AOA, but, conversely, had fewer hemecontaining proteins and more copper-containing proteins than other AOA. Most of the distinctive AR1 and AR2 genes were located in genomic islands (GIs) that were not present in other AOA genomes or in a reference water-column metagenome from the Sargasso Sea. A putative gene cluster involved in urea utilization was found in the AR2 genome, but not the AR1 genome, suggesting niche specialization in marine AOA. Co-cultured bacterial genome analysis suggested that bacterial sulfur and nitrogen metabolism could be involved in interactions with AOA. Our results provide fundamental information concerning the metabolic potential of deep marine sedimentary AOA.
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Although emerging evidence indicates that deep-sea water contains an untapped reservoir of high metabolic and genetic diversity, this realm has not been studied well compared with surface sea water. The study provided the first integrated meta-genomic and -transcriptomic analysis of the microbial communities in deep-sea water of North Pacific Ocean. DNA/RNA amplifications and simultaneous metagenomic and metatranscriptomic analyses were employed to discover information concerning deep-sea microbial communities from four different deep-sea sites ranging from the mesopelagic to pelagic ocean. Within the prokaryotic community, bacteria is absolutely dominant (~90%) over archaea in both metagenomic and metatranscriptomic data pools. The emergence of archaeal phyla Crenarchaeota, Euryarchaeota, Thaumarchaeota, bacterial phyla Actinobacteria, Firmicutes, sub-phyla Betaproteobacteria, Deltaproteobacteria, and Gammaproteobacteria, and the decrease of bacterial phyla Bacteroidetes and Alphaproteobacteria are the main composition changes of prokaryotic communities in the deep-sea water, when compared with the reference Global Ocean Sampling Expedition (GOS) surface water. Photosynthetic Cyanobacteria exist in all four metagenomic libraries and two metatranscriptomic libraries. In Eukaryota community, decreased abundance of fungi and algae in deep sea was observed. RNA/DNA ratio was employed as an index to show metabolic activity strength of microbes in deep sea. Functional analysis indicated that deep-sea microbes are leading a defensive lifestyle.
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Author(s): Leon-Zayas, Rosa Iris | Abstract: This dissertation presents the analyses of twenty-eight single amplified genomes (SAGs) distributed among four major phyla or candidate phyla of archaea and bacteria : Thaumarchaeota, Proteobacteria, Parcubacteria and Marinimicrobia. Samples were obtained from 8,219 m and 10, 908 m depth within the hadal ecosystems of the Puerto Rico Trench (PRT) and Challenger Deep (CHDE) portion of the Mariana Trench, respectively, and microbes associated with seawater, invertebrates and surficial sediments were sorted, amplified by multiple displacement amplification and sequenced using the HiSeq 2000 Illumina platform. Assembled and annotated genomes were analyzed and compared to genomes derived from closely related microbes from other habitats with the goal of understanding PRT and CHDE microbes' metabolic adaptations to deep-sea conditions. Four single amplified genomes (SAGs) were recovered from the PRT: PRT Nitrosopumilus, PRT SAR11, PRT Marin...
Niche Partitioning of the N Cycling Microbial Community of an Offshore Oxygen Deficient Zone
Frontiers in microbiology, 2017
Microbial communities in marine oxygen deficient zones (ODZs) are responsible for up to half of marine N loss through conversion of nutrients to NO and N. This N loss is accomplished by a consortium of diverse microbes, many of which remain uncultured. Here, we characterize genes for all steps in the anoxic N cycle in metagenomes from the water column and >30 μm particles from the Eastern Tropical North Pacific (ETNP) ODZ. We use an approach that allows for both phylogenetic identification and semi-quantitative assessment of gene abundances from individual organisms, and place these results in context of chemical measurements and rate data from the same location. Denitrification genes were enriched in >30 μm particles, even in the oxycline, while anammox bacteria were not abundant on particles. Many steps in denitrification were encoded by multiple phylotypes with different distributions. Notably three NO reductases (), each with no cultured relative, inhabited distinct niches...
Novel bacterial group potentially dominates sulfur cycling in the dark ocean
The dark ocean (>200 m depth) is the largest habitat on Earth. Dissolved inorganic carbon (DIC) fixation in the oxygenated waters of the dark ocean is in the same order of magnitude as heterotrophic microbial biomass production 1,2. Recent evidence suggests sulfur oxidation could be a major energy source for deep ocean microbes 3. However, the global relevance and the identity of the major players in sulfur oxidation in the oxygenated deep-water column remain elusive. Here we combined single-cell genomics, community metagenomics, metatranscriptomics and single-cell activity measurements to present a novel, ubiquitous mixotrophic bacterial group (UBA868) dominating the total expression of RuBisCO genes (up to 40%) and of key sulfur oxidation (soxB and rdsrA) genes (up to 100%) in the global dark ocean. Our study also underscores the unrecognized importance of mixotrophic microbes, such as UBA868, in the biogeochemical cycles of the deep ocean.