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Genomic and enzymatic evidence for acetogenesis among multiple lineages of the archaeal phylum Bathyarchaeota widespread in marine sediments

Nature Microbiology volume 1, Article number: 16035 (2016) Cite this article

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Abstract

Members of the archaeal phylum Bathyarchaeota are widespread and abundant in the energy-deficient marine subsurface sediments. However, their life strategies have remained largely elusive. Here, we provide genetic evidence that some lineages of Bathyarchaeota are acetogens, being capable of homoacetogenesis, a metabolism so far restricted to the domain Bacteria. Metabolic reconstruction based on genomic bins assembled from the metagenome of deep-sea subsurface sediments shows that the metabolism of some lineages of Bathyarchaeota is similar to that of bona fide bacterial homoacetogens, by having pathways for acetogenesis and for the fermentative utilization of a variety of organic substrates. Heterologous expression and activity assay of the acetate kinase gene ack from Bathyarchaeota, demonstrate further the capability of these Bathyarchaeota to grow as acetogens. The presence and expression of bathyarchaeotal genes indicative of active acetogenesis was also confirmed in Peru Margin subsurface sediments where Bathyarchaeota are abundant. The analyses reveal that this ubiquitous and abundant subsurface archaeal group has adopted a versatile life strategy to make a living under energy-limiting conditions. These findings further expand the metabolic potential of Archaea and argue for a revision of the role of Archaea in the carbon cycle of marine sediments.

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Figure 1: Phylogenetic trees showing the placement of genomic bins in the archaeal phylum Bathyarchaeota.
Figure 2: Overview of pathways reconstructed in Bathyarchaeota.
Figure 3: Phylogenies of key genes known to be involved in acetogenesis.
Figure 4: Proposed roles of acetogenic archaea in the deep biosphere.

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Acknowledgements

The authors thank R. Thauer for critical reading of the manuscript, chief scientist C. Vetriani for logistical support, as well as the officers, crew and pilots of R/V Atlantis and DSV Alvin for their expert help at sea. This work has been financially supported by the Natural Science Foundation of China (grant numbers 91228201, 31290232, 41525011 and 41506163), the China Ocean Mineral Resources R&D Association (grant DY125-15-T-04), the Natural Science Foundation of Guangdong and Shenzhen of China (grant numbers 2014A030310056 and JCY20140828163633985) and the US National Science Foundation (grant numbers MCB-0456689 and MCB-0702677 to S.M.S.).

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  1. Y. He and M. Li: These authors contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, China

    Y. He, V. Perumal, X. Feng, J. Fang, J. Xie & F. Wang

  2. State Key Laboratory of Ocean Engineering, Shanghai Jiao Tong University, Shanghai, China

    Y. He & F. Wang

  3. Institute for Advanced Study, Shenzhen University, Shenzhen, Guangdong, China

    M. Li

  4. Biology Department, Woods Hole Oceanographic Institution, Woods Hole, 02543, Massachusetts, USA

    S. M. Sievert

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Contributions

Y.H., M.L., S.M.S. and F.W. designed the experiment and analysis, and interpreted the data. S.M.S. carried out sampling and preservation. V.P. prepared samples for nucleic acid extractions and sequencing, and performed quantitative PCR. Y.H., M.L., X.F. and J.F. performed the bioinformatics analyses. J.X. conducted the protein expression, purification and enzyme assay. Y.H., M.L., S.M.S. and F.W. wrote the manuscript, in consultation with all other authors.

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Correspondence to F. Wang.

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He, Y., Li, M., Perumal, V. et al. Genomic and enzymatic evidence for acetogenesis among multiple lineages of the archaeal phylum Bathyarchaeota widespread in marine sediments. Nat Microbiol 1, 16035 (2016). https://doi.org/10.1038/nmicrobiol.2016.35

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