Original Article | Published:

Bacteria alone establish the chemical basis of the wood-fall chemosynthetic ecosystem in the deep-sea

The ISME Journal volume 12, pages 367379 (2018) | Download Citation

Abstract

Wood-fall ecosystems host chemosynthetic bacteria that use hydrogen sulfide as an electron donor. The production of hydrogen sulfide from decaying wood in the deep-sea has long been suspected to rely on the activity of wood-boring bivalves, Xylophaga spp. However, recent mesocosm experiments have shown hydrogen sulfide production in the absence of wood borers. Here, we combined in situ chemical measurements, amplicon sequencing and metagenomics to test whether the presence of Xylophaga spp.-affected hydrogen sulfide production and wood microbial community assemblages. During a short-term experiment conducted in a deep-sea canyon, we found that wood-fall microbial communities could produce hydrogen sulfide in the absence of Xylophaga spp. The presence of wood borers had a strong impact on the microbial community composition on the wood surface but not in the wood centre, where communities were observed to be homogeneous among different samples. When wood borers were excluded, the wood centre community did not have the genetic potential to degrade cellulose or hemicellulose but could use shorter carbohydrates such as sucrose. We conclude that wood centre communities produce fermentation products that can be used by the sulfate-reducing bacteria detected near the wood surface. We thus demonstrate that microorganisms alone could establish the chemical basis essential for the recruitment of chemolithotrophic organisms in deep-sea wood falls.

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Acknowledgements

The present work was supported by the Agence Nationale de la Recherche (ANR) project MICADO (ANR-11JSV7-Q23-003-01), the UPMC and Fondation TOTAL as part of the chair ‘Extreme marine environments, Biodiversity, and Global change’ and by the CNRS GDRE DIWOOD. We thank the crew of the R/V ‘Minibex’ (COMEX) for their assistance during fieldwork. We are grateful to Julie Rius and Benjamin Falgas from the ‘Biodiversarium’ in Banyuls sur Mer for their kind and precious help in providing pine wood and Yannick Banuls from the laboratory carpentry for precisely cutting the wood logs.

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  1. Sorbonne Universités, UPMC Univ Paris 06, CNRS, Laboratoire d’Ecogéochimie des Environnements Benthiques (LECOB), Observatoire Océanologique, Banyuls sur Mer, France

    • Dimitri Kalenitchenko
    • , Nadine Le Bris
    • , Laetitia Dadaglio
    • , Erwan Peru
    •  & Pierre E Galand
  2. Université de Lorraine, Laboratoire d’étude du matériau bois (LERMAB), Campus bois, Epinal, France

    • Arnaud Besserer

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The authors declare no conflict of interest.

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Correspondence to Dimitri Kalenitchenko.

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https://doi.org/10.1038/ismej.2017.163

Supplementary Information accompanies this paper on The ISME Journal website (http://www.nature.com/ismej)