Dataset Information

Single-Cell Genome and Group-Specific dsrAB Sequencing Implicate Marine Members of the Class Dehalococcoidia (Phylum Chloroflexi) in Sulfur Cycling.

ABSTRACT: UNLABELLED:The marine subsurface sediment biosphere is widely inhabited by bacteria affiliated with the class Dehalococcoidia (DEH), phylum Chloroflexi, and yet little is known regarding their metabolisms. In this report, genomic content from a single DEH cell (DEH-C11) with a 16S rRNA gene that was affiliated with a diverse cluster of 16S rRNA gene sequences prevalent in marine sediments was obtained from sediments of Aarhus Bay, Denmark. The distinctive gene content of this cell suggests metabolic characteristics that differ from those of known DEH and Chloroflexi The presence of genes encoding dissimilatory sulfite reductase (Dsr) suggests that DEH could respire oxidized sulfur compounds, although Chloroflexi have never been implicated in this mode of sulfur cycling. Using long-range PCR assays targeting DEH dsr loci, dsrAB genes were amplified and sequenced from various marine sediments. Many of the amplified dsrAB sequences were affiliated with the DEH Dsr clade, which we propose equates to a family-level clade. This provides supporting evidence for the potential for sulfite reduction by diverse DEH species. DEH-C11 also harbored genes encoding reductases for arsenate, dimethyl sulfoxide, and halogenated organics. The reductive dehalogenase homolog (RdhA) forms a monophyletic clade along with RdhA sequences from various DEH-derived contigs retrieved from available metagenomes. Multiple facts indicate that this RdhA may not be a terminal reductase. The presence of other genes indicated that nutrients and energy may be derived from the oxidation of substituted homocyclic and heterocyclic aromatic compounds. Together, these results suggest that marine DEH play a previously unrecognized role in sulfur cycling and reveal the potential for expanded catabolic and respiratory functions among subsurface DEH. IMPORTANCE:Sediments underlying our oceans are inhabited by microorganisms in cell numbers similar to those estimated to inhabit the oceans. Microorganisms in sediments consist of various diverse and uncharacterized groups that contribute substantially to global biogeochemical cycles. Since most subsurface microorganisms continue to evade cultivation, possibly due to very slow growth, we obtained and analyzed genomic information from a representative of one of the most widespread and abundant, yet uncharacterized bacterial groups of the marine subsurface. We describe several key features that may contribute to their widespread distribution, such as respiratory flexibility and the potential to use oxidized sulfur compounds, which are abundant in marine environments, as electron acceptors. Together, these data provide important information that can be used to assist in designing enrichment strategies or other postgenomic studies, while also improving our understanding of the diversity and distribution of dsrAB genes, which are widely used functional marker genes for sulfur-cycling microbes.

SUBMITTER: Wasmund K

PROVIDER: S-EPMC4959651 | biostudies-literature | 2016 May

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Single-Cell Genome and Group-Specific dsrAB Sequencing Implicate Marine Members of the Class Dehalococcoidia (Phylum Chloroflexi) in Sulfur Cycling.

Wasmund Kenneth K Cooper Myriel M Schreiber Lars L Lloyd Karen G KG Baker Brett J BJ Petersen Dorthe G DG Jørgensen Bo Barker BB Stepanauskas Ramunas R Reinhardt Richard R Schramm Andreas A Loy Alexander A Adrian Lorenz L

mBio 20160503 3

<h4>Unlabelled</h4>The marine subsurface sediment biosphere is widely inhabited by bacteria affiliated with the class Dehalococcoidia (DEH), phylum Chloroflexi, and yet little is known regarding their metabolisms. In this report, genomic content from a single DEH cell (DEH-C11) with a 16S rRNA gene that was affiliated with a diverse cluster of 16S rRNA gene sequences prevalent in marine sediments was obtained from sediments of Aarhus Bay, Denmark. The distinctive gene content of this cell sugges ...[more]

PMID: 27143384

Similar Datasets

Project description:BACKGROUND: Sediments are massive reservoirs of carbon compounds and host a large fraction of microbial life. Microorganisms within terrestrial aquifer sediments control buried organic carbon turnover, degrade organic contaminants, and impact drinking water quality. Recent 16S rRNA gene profiling indicates that members of the bacterial phylum Chloroflexi are common in sediment. Only the role of the class Dehalococcoidia, which degrade halogenated solvents, is well understood. Genomic sampling is available for only six of the approximate 30 Chloroflexi classes, so little is known about the phylogenetic distribution of reductive dehalogenation or about the broader metabolic characteristics of Chloroflexi in sediment. RESULTS: We used metagenomics to directly evaluate the metabolic potential and diversity of Chloroflexi in aquifer sediments. We sampled genomic sequence from 86 Chloroflexi representing 15 distinct lineages, including members of eight classes previously characterized only by 16S rRNA sequences. Unlike in the Dehalococcoidia, genes for organohalide respiration are rare within the Chloroflexi genomes sampled here. Near-complete genomes were reconstructed for three Chloroflexi. One, a member of an unsequenced lineage in the Anaerolinea, is an aerobe with the potential for respiring diverse carbon compounds. The others represent two genomically unsampled classes sibling to the Dehalococcoidia, and are anaerobes likely involved in sugar and plant-derived-compound degradation to acetate. Both fix CO2 via the Wood-Ljungdahl pathway, a pathway not previously documented in Chloroflexi. The genomes each encode unique traits apparently acquired from Archaea, including mechanisms of motility and ATP synthesis. CONCLUSIONS: Chloroflexi in the aquifer sediments are abundant and highly diverse. Genomic analyses provide new evolutionary boundaries for obligate organohalide respiration. We expand the potential roles of Chloroflexi in sediment carbon cycling beyond organohalide respiration to include respiration of sugars, fermentation, CO2 fixation, and acetogenesis with ATP formation by substrate-level phosphorylation.

Project description:A key component of the marine sulfur cycle is the climate-active gas dimethylsulfide (DMS), which is synthesized by a range of organisms from phytoplankton to corals, and accounts for up to 80% of global biogenic sulfur emissions. The DMS cycle starts with the intracellular synthesis of the non-gaseous precursor dimethylsulfoniopropionate (DMSP), which is released to the water column by various food web processes such as zooplankton grazing. This dissolved DMSP pool is rapidly turned over by microbially mediated conversion using two known pathways: demethylation (releasing methanethiol) and cleavage (producing DMS). Some of the formed DMS is ventilated to the atmosphere, where it undergoes rapid oxidation and contributes to the formation of sulfate aerosols, with the potential to affect cloud microphysics, and thus the regional climate. The marine phase cycling of DMS is complex, however, as heterotrophs also contribute to the consumption of the newly formed dissolved DMS. Interestingly, due to microbial consumption and other water column sinks such as photolysis, the amount of DMS that enters the atmosphere is currently thought to be a relatively minor fraction of the total amount cycled through the marine food web-less than 10%. These microbial processes are mediated by water column temperature, but the response of marine microbial assemblages to ocean warming is poorly characterized, although bacterial degradation appears to increase with an increase in temperature. This review will focus on the potential impact of climate change on the key microbially mediated processes in the marine cycling of DMS. It is likely that the impact will vary across different biogeographical regions from polar to tropical. For example, in the rapidly warming polar oceans, microbial communities associated with the DMS cycle will likely change dramatically during the 21st century with the decline in sea ice. At lower latitudes, where corals form an important source of DMS (P), shifts in the microbiome composition have been observed during thermal stress with the potential to alter the DMS cycle.

Project description:Marine fjords with active glacier outlets are hot spots for organic matter burial in the sediments and subsequent microbial mineralization. Here, we investigated controls on microbial community assembly in sub-arctic glacier-influenced (GI) and non-glacier-influenced (NGI) marine sediments in the Godthåbsfjord region, south-western Greenland. We used a correlative approach integrating 16S rRNA gene and dissimilatory sulfite reductase (dsrB) amplicon sequence data over six meters of depth with biogeochemistry, sulfur-cycling activities, and sediment ages. GI sediments were characterized by comparably high sedimentation rates and had "young" sediment ages of <500 years even at 6 m sediment depth. In contrast, NGI stations reached ages of approximately 10,000 years at these depths. Sediment age-depth relationships, sulfate reduction rates (SRR), and C/N ratios were strongly correlated with differences in microbial community composition between GI and NGI sediments, indicating that age and diagenetic state were key drivers of microbial community assembly in subsurface sediments. Similar bacterial and archaeal communities were present in the surface sediments of all stations, whereas only in GI sediments were many surface taxa also abundant through the whole sediment core. The relative abundance of these taxa, including diverse Desulfobacteraceae members, correlated positively with SRRs, indicating their active contributions to sulfur-cycling processes. In contrast, other surface community members, such as Desulfatiglans, Atribacteria, and Chloroflexi, survived the slow sediment burial at NGI stations and dominated in the deepest sediment layers. These taxa are typical for the energy-limited marine deep biosphere and their relative abundances correlated positively with sediment age. In conclusion, our data suggests that high rates of sediment accumulation caused by glacier runoff and associated changes in biogeochemistry, promote persistence of sulfur-cycling activity and burial of a larger fraction of the surface microbial community into the deep subsurface.

Dataset Information

Single-Cell Genome and Group-Specific dsrAB Sequencing Implicate Marine Members of the Class Dehalococcoidia (Phylum Chloroflexi) in Sulfur Cycling.

Publications

Single-Cell Genome and Group-Specific dsrAB Sequencing Implicate Marine Members of the Class Dehalococcoidia (Phylum Chloroflexi) in Sulfur Cycling.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets