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Functional shifts in microbial mats recapitulate early Earth metabolic transitions

Nature Ecology & Evolution volume 2, pages 1700–1708 (2018)Cite this article

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Abstract

Phototrophic microbial mats dominated terrestrial ecosystems for billions of years, largely causing, through cyanobacterial oxygenic photosynthesis, but also undergoing, the Great Oxidation Event approximately 2.5 billion years ago. Taking a space-for-time approach based on the universality of core metabolic pathways expressed at ecosystem level, we studied gene content and co-occurrence networks in high-diversity metagenomes from spatially close microbial mats along a steep redox gradient. The observed functional shifts suggest that anoxygenic photosynthesis was present but not predominant under early Precambrian conditions, being accompanied by other autotrophic processes. Our data also suggest that, in contrast to general assumptions, anoxygenic photosynthesis largely expanded in parallel with the subsequent evolution of oxygenic photosynthesis and aerobic respiration. Finally, our observations might represent space-for-time evidence that the Wood–Ljungdahl carbon fixation pathway dominated phototrophic mats in early ecosystems, whereas the Calvin cycle probably evolved from pre-existing variants before becoming the dominant contemporary form of carbon fixation.

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Fig. 1: Microbial diversity in microbial mat metagenomes along a redox gradient in a pond from the Salar de Llamara (Atacama Desert, Chile).
Fig. 2: Major energy and carbon metabolisms in Llamara microbial mats based on diagnostic genes.
Fig. 3: Co-occurrence networks of diagnostic KOs involved in major energy and carbon fixation metabolic pathways in Llamara microbial mats from pond LLA9.
Fig. 4: Distribution of key energy and carbon fixation metabolisms in microbial mats across a redox gradient and, probably, time.

Data availability

The sequence datasets of the Llamara metagenomes have been deposited in GenBank with the BioProject accession code PRJNA438773 (corresponding to BioSample accessions SAMN08688543 to SAMN08688553). All codes generated for this study are available at Gitlab https://gitlab.com/DeemTeam/LLA9-Metagenomes. To facilitate colour identification in figures, numbers used to build all histograms are provided in the supplementary file Tables_for_Figures.xlsx

Change history

  • 05 November 2018

    In the version of this Article originally published, Supplementary Data 1 was incorrectly linked to Supplementary Table 8, Supplementary Table 1 was incorrectly linked to Supplementary Table 5, Supplementary Table 2 was incorrectly linked to Supplementary Data 1, Supplementary Table 3 was incorrectly linked to Supplementary Table 1, Supplementary Table 4 was incorrectly linked to Supplementary Table 2, Supplementary Table 5 was incorrectly linked to Supplementary Table 3, Supplementary Table 6 was incorrectly linked to Supplementary Table 4, and Supplementary Table 8 was incorrectly linked to Supplementary Table 6. The files have now been replaced to rectify this.

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Acknowledgements

We thank R. Rodríguez de la Vega for discussions about bioinformatics tools, J. Friedman for advice on SparCC, A. Abdala for helping with MySQL database reconstruction and E. Merino for help in COG assignation. We also thank I. Aracena (Departamento de Medio Ambiente, Sociedad Química y Minera, Chile), J. M. López-García (Instituto Geológico y Minero de España) and J. M. García-Ruiz’s team (Universidad de Granada) for sampling access, georeferencing, and company during the field trip. This research was funded by the European Research Council grant no. 322669 to P.L.G. under the European Union’s Seventh Framework Programme.

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Author notes

  1. These authors contributed equally: Ana Gutiérrez-Preciado, Aurélien Saghaï.

Authors and Affiliations

  1. Ecologie Systématique Evolution, CNRS, Université Paris-Sud, AgroParisTech, Université Paris-Saclay, Orsay, France

    Ana Gutiérrez-Preciado, Aurélien Saghaï, David Moreira, Philippe Deschamps & Purificación López-García

  2. Institut de Biologie Intégrative de la Cellule, CNRS, Université Paris-Sud, Université Paris-Saclay, Orsay, France

    Yvan Zivanovic

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  1. Ana Gutiérrez-Preciado
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Contributions

A.G.-P. and A.S. performed the bioinformatic analyses, analysed the data and wrote a preliminary draft of the manuscript. Y.Z. supervised initial metagenome assembly and annotation. P.D. helped with software installation and use. D.M. and P.L.G. collected the samples and conceived the study. P.L.G. prepared the samples for sequencing, supervised the work, provided hypotheses and wrote the final manuscript.

Corresponding author

Correspondence to Purificación López-García.

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Supplementary information

Supplementary Figures

Supplementary Figures 1–11.

Reporting Summary

Supplementary Data 1

Tables with the values used to build colour histograms in the manuscript.

Supplementary Table 1

Assembly and annotation statistics of the 11 metagenomes of the microbial mat layers from Llamara.

Supplementary Table 2

Distribution of clusters of orthologous genes (COGs) in Llamara microbial mats.

Supplementary Table 3

Distribution of PFAMs in the different Llamara microbial mats.

Supplementary Table 4

Distribution of KEGG orthologues (KOs) in the different Llamara microbial mats.

Supplementary Table 5

Single copy gene families (COGs) universally distributed in prokaryotic genomes used to characterize the phylogenetic composition of microbial communities in Llamara microbial mats.

Supplementary Table 6

Single copy gene families (PFAMs) universally distributed in bacteria and archaea used to characterize the phylogenetic composition of prokaryotic communities in Llamara microbial mats.

Supplementary Table 7

Diagnostic KOs used for network analyses.

Supplementary Table 8

Network properties.

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Gutiérrez-Preciado, A., Saghaï, A., Moreira, D. et al. Functional shifts in microbial mats recapitulate early Earth metabolic transitions. Nat Ecol Evol 2, 1700–1708 (2018). https://doi.org/10.1038/s41559-018-0683-3

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