An archaea-specific c-type cytochrome maturation machinery is crucial for methanogenesis in Methanosarcina acetivorans

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Abstract

C-type cytochromes (cyt c) are proteins that undergo post-translational modification to covalently bind heme, which allows them to facilitate redox reactions in electron transport chains across all domains of life. Genomic evidence suggests that cyt c are involved in electron transfer processes among the Archaea, especially in members that produce or consume the potent greenhouse gas methane. However, neither the maturation machinery for cyt c in Archaea nor their role in methane metabolism has ever been functionally characterized. Here, we have used CRISPR-Cas9 genome editing tools to map a distinct pathway for cyt c biogenesis in the model methanogenic archaeon Methanosarcina acetivorans, and have also identified substrate-specific functional roles for cyt c during methanogenesis. Although the cyt c maturation machinery from M. acetivorans is universally conserved in the Archaea, our evolutionary analyses indicate that different clades of Archaea acquired this machinery through multiple independent horizontal gene transfer events from different groups of Bacteria. Overall, we demonstrate the convergent evolution of a novel Archaea-specific cyt c maturation machinery and its physiological role during methanogenesis, a process which contributes substantially to global methane emissions

Data availability

All data generated or analysed during this study are included in the manuscript and supporting file; Sequencing data have been deposited in the NCBI SRA (Sequence Read Archive) under bioproject number PRJNA800036. Source data files for Figure1b, Figure 2c, Figure 3d, Figure 4c and Figure 3- Figure Supplement 1, Figure 4 - Figure Supplement 1 and 2, are provided.

The following data sets were generated

(2022) Whole genome re-sequencing data for the Methanosarcina acetivorans ccmABC deletion mutant
NCBI SRA , PRJNA800036.

https://www.ncbi.nlm.nih.gov/sra/?term=PRJNA800036

Article and author information

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Dinesh Gupta

Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-9108-9669
Katie E Shalvarjian

Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States

Competing interests
The authors declare that no competing interests exist.
Dipti D Nayak

Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States

For correspondence
dnayak@berkeley.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-3449-3419

Funding

Gordon and Betty Moore Foundation (GBMF#9324)

Dipti D Nayak

Gordon and Betty Moore Foundation (GBMF#9324)

Dinesh Gupta

Simons Foundation (imons Early Career Investigator in Marine Microbial Ecology and Evolution Award (822981))

Dipti D Nayak

Simons Foundation (imons Early Career Investigator in Marine Microbial Ecology and Evolution Award (822981))

Katie E Shalvarjian

David and Lucile Packard Foundation (Packard Fellowships for Science and Engineering)

Dipti D Nayak

Searle Scholars Program (Searle Scholars Program)

Dipti D Nayak

Arnold and Mabel Beckman Foundation (Beckman Young Investigator Program)

Dipti D Nayak

Shurl and Kay Curci Foundation

Dipti D Nayak

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.