Dataset Information

Turnover of microbial lipids in the deep biosphere and growth of benthic archaeal populations.

ABSTRACT: Deep subseafloor sediments host a microbial biosphere with unknown impact on global biogeochemical cycles. This study tests previous evidence based on microbial intact polar lipids (IPLs) as proxies of live biomass, suggesting that Archaea dominate the marine sedimentary biosphere. We devised a sensitive radiotracer assay to measure the decay rate of ([(14)C]glucosyl)-diphytanylglyceroldiether (GlcDGD) as an analog of archaeal IPLs in continental margin sediments. The degradation kinetics were incorporated in model simulations that constrained the fossil fraction of subseafloor IPLs and rates of archaeal turnover. Simulating the top 1 km in a generic continental margin sediment column, we estimated degradation rate constants of GlcDGD being one to two orders of magnitude lower than those of bacterial IPLs, with half-lives of GlcDGD increasing with depth to 310 ky. Given estimated microbial community turnover times of 1.6-73 ky in sediments deeper than 1 m, 50-96% of archaeal IPLs represent fossil signals. Consequently, previous lipid-based estimates of global subseafloor biomass probably are too high, and the widely observed dominance of archaeal IPLs does not rule out a deep biosphere dominated by Bacteria. Reverse modeling of existing concentration profiles suggest that archaeal IPL synthesis rates decline from around 1,000 pg?mL(-1) sediment?y(-1) at the surface to 0.2 pg?mL(-1)?y(-1) at 1 km depth, equivalent to production of 7 × 10(5) to 140 archaeal cells?mL(-1) sediment?y(-1), respectively. These constraints on microbial growth are an important step toward understanding the relationship between the deep biosphere and the carbon cycle.

SUBMITTER: Xie S

PROVIDER: S-EPMC3625344 | biostudies-literature | 2013 Apr

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Turnover of microbial lipids in the deep biosphere and growth of benthic archaeal populations.

Xie Sitan S Lipp Julius S JS Wegener Gunter G Ferdelman Timothy G TG Hinrichs Kai-Uwe KU

Proceedings of the National Academy of Sciences of the United States of America 20130325 15

Deep subseafloor sediments host a microbial biosphere with unknown impact on global biogeochemical cycles. This study tests previous evidence based on microbial intact polar lipids (IPLs) as proxies of live biomass, suggesting that Archaea dominate the marine sedimentary biosphere. We devised a sensitive radiotracer assay to measure the decay rate of ([(14)C]glucosyl)-diphytanylglyceroldiether (GlcDGD) as an analog of archaeal IPLs in continental margin sediments. The degradation kinetics were i ...[more]

PMID: 23530229

Similar Datasets

Project description:Benthic environments harbor highly diverse and complex microbial communities that control carbon fluxes, but the role of specific uncultivated microbial groups in organic matter turnover is poorly understood. In this study, quantitative DNA stable isotope probing (DNA-qSIP) was used for the first time to link uncultivated populations of bacteria and archaea to carbon turnover in lacustrine surface sediments. After 1-week incubations in the dark with [13C]bicarbonate, DNA-qSIP showed that ammonia-oxidizing archaea (AOA) were the dominant active chemolithoautotrophs involved in the production of new organic matter. Natural 13C-labeled organic matter was then obtained by incubating sediments in the dark for 2.5 months with [13C]bicarbonate, followed by extraction and concentration of high-molecular-weight (HMW) (>50-kDa) organic matter. qSIP showed that the labeled organic matter was turned over within 1 week by 823 microbial populations (operational taxonomic units [OTUs]) affiliated primarily with heterotrophic Proteobacteria, Chloroflexi, Verrucomicrobia, and Bacteroidetes However, several OTUs affiliated with the candidate microbial taxa Latescibacteria, Omnitrophica, Aminicentantes, Cloacimonates, AC1, Bathyarchaeota, and Woesearchaeota, groups known only from genomic signatures, also contributed to biomass turnover. Of these 823 labeled OTUs, 52% (primarily affiliated with Proteobacteria) also became labeled in 1-week incubations with [13C]bicarbonate, indicating that they turned over carbon faster than OTUs that were labeled only in incubations with 13C-labeled HMW organic matter. These taxa consisted primarily of uncultivated populations within the Firmicutes, Bacteroidetes, Verrucomicrobia, and Chloroflexi, highlighting their ecological importance. Our study helps define the role of several poorly understood, uncultivated microbial groups in the turnover of benthic carbon derived from "dark" primary production.IMPORTANCE Little is known about the ecological role of uncultivated microbial populations in carbon turnover in benthic environments. To better understand this, we used quantitative stable isotope probing (qSIP) to quantify the abundance of diverse, specific groups of uncultivated bacteria and archaea involved in autotrophy and heterotrophy in a benthic lacustrine habitat. Our results provide quantitative evidence for active heterotrophic and autotrophic metabolism of several poorly understood microbial groups, thus demonstrating their relevance for carbon turnover in benthic settings. Archaeal ammonia oxidizers were significant drivers of in situ "dark" primary production supporting the growth of heterotrophic bacteria. These findings expand our understanding of the microbial populations within benthic food webs and the role of uncultivated microbes in benthic carbon turnover.

Project description:Archaea are widespread in marine sediments and play important roles in the cycling of sedimentary organic carbon. However, factors controlling the distribution of archaea in marine sediments are not well understood. Here we investigated benthic archaeal communities over glacial-interglacial cycles in the northern South China Sea and evaluated their responses to sediment organic matter sources and inter-species interactions. Archaea in sediments deposited during the interglacial period Marine Isotope Stage (MIS) 1 (Holocene) were significantly different from those in sediments deposited in MIS 2 and MIS 3 of the Last Glacial Period when terrestrial input to the South China Sea was enhanced based on analysis of the long-chain n-alkane C31. The absolute archaeal 16S rRNA gene abundance in subsurface sediments was highest in MIS 2, coincident with high sedimentation rates and high concentrations of total organic carbon. Soil Crenarchaeotic Group (SCG; Nitrososphaerales) species, the most abundant ammonia-oxidizing archaea in soils, increased dramatically during MIS 2, likely reflecting transport of terrestrial archaea during glacial periods with high sedimentation rates. Co-occurrence network analyses indicated significant association of SCG archaea with benthic deep-sea microbes such as Bathyarchaeota and Thermoprofundales in MIS 2 and MIS 3, suggesting potential interactions among these archaeal groups. Meanwhile, Thermoprofundales abundance was positively correlated with total organic carbon (TOC), along with n-alkane C31 and sedimentation rate, indicating that Thermoprofundales may be particularly important in processing of organic carbon in deep-sea sediments. Collectively, these results demonstrate that the composition of heterotrophic benthic archaea in the South China Sea may be influenced by terrestrial organic input in tune with glacial-interglacial cycles, suggesting a plausible link between global climate change and microbial population dynamics in deep-sea marine sediments.

Dataset Information

Turnover of microbial lipids in the deep biosphere and growth of benthic archaeal populations.

Publications

Turnover of microbial lipids in the deep biosphere and growth of benthic archaeal populations.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets