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Resource partitioning among brachiopods and bivalves at ancient hydrocarbon seeps: A hypothesis.

ABSTRACT: Brachiopods were thought to have dominated deep-sea hydrothermal vents and hydrocarbon seeps for most of the Paleozoic and Mesozoic, and were believed to have been outcompeted and replaced by chemosymbiotic bivalves during the Late Cretaceous. But recent findings of bivalve-rich seep deposits of Paleozoic and Mesozoic age have questioned this paradigm. By tabulating the generic diversity of the dominant brachiopod and bivalve clades-dimerelloid brachiopods and chemosymbiotic bivalves-from hydrocarbon seeps through the Phanerozoic, we show that their evolutionary trajectories are largely unrelated to one another, indicating that they have not been competing for the same resources. We hypothesize that the dimerelloid brachiopods generally preferred seeps with abundant hydrocarbons in the bottom waters above the seep, such as oil seeps or methane seeps with diffusive seepage, whereas seeps with strong, advective fluid flow and hence abundant hydrogen sulfide were less favorable for them. At methane seeps typified by diffusive seepage and oil seeps, oxidation of hydrocarbons in the bottom water by chemotrophic bacteria enhances the growth of bacterioplankton, on which the brachiopods could have filter fed. Whereas chemosymbiotic bivalves mostly relied on sulfide-oxidizing symbionts for nutrition, for the brachiopods aerobic bacterial oxidation of methane and other hydrocarbons played a more prominent role. The availability of geofuels (i.e. the reduced chemical compounds used in chemosynthesis such as hydrogen sulfide, methane, and other hydrocarbons) at seeps is mostly governed by fluid flow rates, geological setting, and marine sulfate concentrations. Thus rather than competition, we suggest that geofuel type and availability controlled the distribution of brachiopods and bivalves at hydrocarbon seeps through the Phanerozoic.

SUBMITTER: Kiel S

PROVIDER: S-EPMC6728048 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Resource partitioning among brachiopods and bivalves at ancient hydrocarbon seeps: A hypothesis.

Kiel Steffen S Peckmann Jörn J

PloS one 20190905 9

Brachiopods were thought to have dominated deep-sea hydrothermal vents and hydrocarbon seeps for most of the Paleozoic and Mesozoic, and were believed to have been outcompeted and replaced by chemosymbiotic bivalves during the Late Cretaceous. But recent findings of bivalve-rich seep deposits of Paleozoic and Mesozoic age have questioned this paradigm. By tabulating the generic diversity of the dominant brachiopod and bivalve clades-dimerelloid brachiopods and chemosymbiotic bivalves-from hydroc ...[more]

PMID: 31487311

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Project description:Marine sediments are important methane reservoirs. Methane efflux from the seabed is significantly restricted by anaerobic methanotrophic (ANME) archaea through a process known as anaerobic oxidation of methane (AOM). Different clades of ANME archaea occupy distinct niches in methane seeps, but their underlying molecular mechanisms still need to be fully understood. To provide genetic explanations for the niche partitioning of ANME archaea, we applied comparative genomic analysis to ANME archaeal genomes retrieved from global methane seeps. Our results showed that ANME-2 archaea are more prevalent than ANME-1 archaea in shallow sediments because they carry genes that encode a significantly higher number of outer membrane multiheme c-type cytochromes and flagellar proteins. These features make ANME-2 archaea perform direct interspecies electron transfer better and benefit more from electron acceptors in AOM. Besides, ANME-2 archaea carry genes that encode extra peroxidase compared to ANME-1 archaea, which may lead to ANME-2 archaea better tolerating oxygen toxicity. In contrast, ANME-1 archaea are more competitive in deep layers than ANME-2 archaea because they carry extra genes (mtb and mtt) for methylotrophic methanogenesis and a significantly higher number of frh and mvh genes for hydrogenotrophic methanogenesis. Additionally, ANME-1 archaea carry exclusive genes (sqr, TST, and mddA) involved in sulfide detoxification compared to ANME-2 archaea, leading to stronger sulfide tolerance. Overall, this study reveals the genomic mechanisms shaping the niche partitioning among ANME archaea in global methane seeps. IMPORTANCE Anaerobic methanotrophic (ANME) archaea are important methanotrophs in marine sediment, controlling the flux of biologically generated methane, which plays an essential role in the marine carbon cycle and climate change. So far, no strain of this lineage has been isolated in pure culture, which makes metagenomics one of the fundamental approaches to reveal their metabolic potential. Although the niche partitioning of ANME archaea was frequently reported in different studies, whether this pattern was consistent in global methane seeps had yet to be verified, and little was known about the genetic mechanisms underlying it. Here, we reviewed and analyzed the community structure of ANME archaea in global methane seeps and indicated that the niche partitioning of ANME archaea was statistically supported. Our comparative genomic analysis indicated that the capabilities of interspecies electron transfer, methanogenesis, and the resistance of oxygen and hydrogen sulfide could be critical in defining the distribution of ANME archaea in methane seep sediment.

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Dataset Information

Resource partitioning among brachiopods and bivalves at ancient hydrocarbon seeps: A hypothesis.

Publications

Resource partitioning among brachiopods and bivalves at ancient hydrocarbon seeps: A hypothesis.

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