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Environmental drivers of a microbial genomic transition zone in the ocean’s interior

Nature Microbiology volume 2, pages 1367–1373 (2017)Cite this article

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Abstract

The core properties of microbial genomes, including GC content and genome size, are known to vary widely among different bacteria and archaea1,2. Several hypotheses have been proposed to explain this genomic variability, but the fundamental drivers that shape bacterial and archaeal genomic properties remain uncertain3,4,5,6,7. Here, we report the existence of a sharp genomic transition zone below the photic zone, where bacterial and archaeal genomes and proteomes undergo a community-wide punctuated shift. Across a narrow range of increasing depth of just tens of metres, diverse microbial clades trend towards larger genome size, higher genomic GC content, and proteins with higher nitrogen but lower carbon content. These community-wide changes in genome features appear to be driven by gradients in the surrounding environmental energy and nutrient fields. Collectively, our data support hypotheses invoking nutrient limitation as a central driver in the evolution of core bacterial and archaeal genomic and proteomic properties.

Major physicochemical features that distinguish the ocean’s twilight zone (mesopelagic zone, 200–1,000 m) from well-lit surface layers include lower light, temperature and oxygen levels, together with higher hydrostatic pressure and macronutrient concentrations. Although some differences between surface and deeper-water microbes are now predictable8,9,10,11, the specific nature of genomic variability along the vertical depth continuum is less clear.

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Fig. 1: Quantitative relationships of microbiome genes and taxa and as a function of depth, time and environmental variables at Station ALOHA.
Fig. 2: Microbiome GC content, N-ARSC and C-ARSC versus depth at Station ALOHA.
Fig. 3: Distribution of taxon modules through the GTZ, and with nitrogen concentrations over time at 125 m.

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Acknowledgements

The authors thank the captain and crew of the R/V Kilo Moana, and the Hawaii Ocean Time-series marine operations team, for their expert assistance with sample collection and oceanographic data acquisition and analyses at sea. The authors also thank T. Palden, A. Romano and P. Den Uyl for their able assistance in DNA library preparation and DNA sequencing, and B. Barone and L. Fujieki for expert advice and assistance in accessing and displaying HOT oceanographic data sets. The authors also thank S. Sunagawa and G. Zeller for advice and assistance with mOTU analyses. This research was supported by the Simons Foundation (SCOPE award ID 329108 to E.F.D. and D.M.K.), the Gordon and Betty Moore Foundation (through grants GBMF 3777 to E.F.D. and GBMF3794 to D.M.K.) and the National Science Foundation for support of the HOT programme (including the most recent OCE1260164), as well as support to D.R.M. from EMBO (ALTF 721-2015) and the European Commission (LTFCOFUND2013, GA-2013-609409) and support to J.A.B. through the US EPA Science to Achieve Results Fellowship. This work is a contribution of the Simons Collaboration on Ocean Processes and Ecology, and the Center for Microbial Oceanography: Research and Education.

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Author notes

  1. Daniel R. Mende, Jessica A. Bryant and Frank O. Aylward contributed equally to this work.

Authors and Affiliations

  1. Daniel K. Inouye Center for Microbial Oceanography: Research and Education (C-MORE), University of Hawaii, Honolulu, HI, 96822, USA

    Daniel R. Mende, Jessica A. Bryant, Frank O. Aylward, John M. Eppley, Torben Nielsen, David M. Karl & Edward F. DeLong

  2. Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA

    Jessica A. Bryant & Edward F. DeLong

  3. DOE Joint Genome Institute, Walnut Creek, CA, 94598, USA

    Torben Nielsen

  4. Department of Biological Sciences, Virginia Tech, Blacksburg, VA, 24061, USA

    Frank O. Aylward

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  1. Daniel R. Mende
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Contributions

E.F.D. and D.M.K. designed the overall study, sample and data collection, and analyses. T.N., J.M.E., D.R.M., J.A.B. and F.O.A. performed bioinformatics analyses with input from E.F.D. The manuscript was written by E.F.D., D.R.M., J.A.B. and F.O.A.

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Correspondence to Edward F. DeLong.

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Supplementary Information

Supplementary Figures 1–10.

Supplementary Table 1

Sequencing and assembly statistics.

Supplementary Table 2

Physicochemical and biological environmental data.

Supplementary Table 3

Chlorophyll measurements.

Supplementary Table 4

SRA database accession information.

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Mende, D.R., Bryant, J.A., Aylward, F.O. et al. Environmental drivers of a microbial genomic transition zone in the ocean’s interior. Nat Microbiol 2, 1367–1373 (2017). https://doi.org/10.1038/s41564-017-0008-3

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