Thermophilic anaerobes in Arctic marine sediments induced to mineralize complex organic matter at high temperature

Authors

  • Casey Hubert,

    Corresponding author
    1. Department of Biogeochemistry, Max Planck Institute for Marine Microbiology, Bremen, Germany.
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    • Present addresses: School of Civil Engineering and Geosciences, Newcastle University, Newcastle Upon Tyne, UK;

  • Carol Arnosti,

    1. Department of Marine Sciences, University of North Carolina, Chapel Hill, NC, USA.
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  • Volker Brüchert,

    1. Department of Biogeochemistry, Max Planck Institute for Marine Microbiology, Bremen, Germany.
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    • Department of Geology and Geochemistry, Stockholm University, Stockholm, Sweden;

  • Alexander Loy,

    1. Department of Microbial Ecology, University of Vienna, Vienna, Austria.
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  • Verona Vandieken,

    1. Department of Biogeochemistry, Max Planck Institute for Marine Microbiology, Bremen, Germany.
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    • §

      Institute of Biology, University of Southern Denmark, Odense, Denmark.

  • Bo Barker Jørgensen

    1. Department of Biogeochemistry, Max Planck Institute for Marine Microbiology, Bremen, Germany.
    2. Center for Geomicrobiology, Aarhus University, Aarhus, Denmark.
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E-mail casey.hubert@newcastle.ac.uk; Tel. (+44) 191 246 4864; Fax (+44) 191 222 6502.

Summary

Marine sediments harbour diverse populations of dormant thermophilic bacterial spores that become active in sediment incubation experiments at much higher than in situ temperature. This response was investigated in the presence of natural complex organic matter in sediments of two Arctic fjords, as well as with the addition of freeze-dried Spirulina or individual high-molecular-weight polysaccharides. During 50°C incubation experiments, Arctic thermophiles catalysed extensive mineralization of the organic matter via extracellular enzymatic hydrolysis, fermentation and sulfate reduction. This high temperature-induced food chain mirrors sediment microbial processes occurring at cold in situ temperatures (near 0°C), yet it is catalysed by a completely different set of microorganisms. Using sulfate reduction rates (SRR) as a proxy for organic matter mineralization showed that differences in organic matter reactivity determined the extent of the thermophilic response. Fjord sediments with higher in situ SRR also supported higher SRR at 50°C. Amendment with Spirulina significantly increased volatile fatty acids production and SRR relative to unamended sediment in 50°C incubations. Spirulina amendment also revealed temporally distinct sulfate reduction phases, consistent with 16S rRNA clone library detection of multiple thermophilic Desulfotomaculum spp. enriched at 50°C. Incubations with four different fluorescently labelled polysaccharides at 4°C and 50°C showed that the thermophilic population in Arctic sediments produce a different suite of polymer-hydrolysing enzymes than those used in situ by the cold-adapted microbial community. Over time, dormant marine microorganisms like these are buried in marine sediments and might eventually encounter warmer conditions that favour their activation. Distinct enzymatic capacities for organic polymer degradation could allow specific heterotrophic populations like these to play a role in sustaining microbial metabolism in the deep, warm, marine biosphere.

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