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The Chloroflexi supergroup is metabolically diverse and representatives have novel genes for non-photosynthesis based CO2 fixation

Jacob A. West-Roberts, View ORCID ProfilePaula B. Matheus-Carnevali, Marie Charlotte Schoelmerich, Basem Al-Shayeb, Alex D. Thomas, Allison Sharrar, View ORCID ProfileChristine He, Lin-Xing Chen, View ORCID ProfileAdi Lavy, Ray Keren, Yuki Amano, Jillian F. Banfield
doi: https://doi.org/10.1101/2021.08.23.457424
Jacob A. West-Roberts
1University of California – Berkeley
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Paula B. Matheus-Carnevali
2University of California, Berkeley
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Marie Charlotte Schoelmerich
2University of California, Berkeley
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Basem Al-Shayeb
2University of California, Berkeley
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Alex D. Thomas
2University of California, Berkeley
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Allison Sharrar
2University of California, Berkeley
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Christine He
2University of California, Berkeley
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Lin-Xing Chen
2University of California, Berkeley
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Adi Lavy
3University of California Berkeley
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Ray Keren
3University of California Berkeley
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Yuki Amano
4Sector of Decommissioning and Radioactive Wastes Management, Japan Atomic Energy Agency
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Jillian F. Banfield
2University of California, Berkeley
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  • For correspondence: jbanfield@berkeley.edu
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Abstract

The Chloroflexi superphylum have been investigated primarily from the perspective of reductive dehalogenation of toxic compounds, anaerobic photosynthesis and wastewater treatment, but remain relatively little studied compared to their close relatives within the larger Terrabacteria group, including Cyanobacteria, Actinobacteria, and Firmicutes. Here, we conducted a detailed phylogenetic analysis of the phylum Chloroflexota, the phylogenetically proximal candidate phylum Dormibacteraeota, and a newly defined sibling phylum proposed in the current study, Eulabeiota. These groups routinely root together in phylogenomic analyses, and constitute the Chloroflexi supergroup. Chemoautotrophy is widespread in Chloroflexi. Two Form I Rubisco ancestral subtypes that both lack the small subunit are prevalent in ca. Eulabeiota and Chloroflexota, suggesting that the predominant modern pathway for CO2 fixation evolved in these groups. The single subunit Form I Rubiscos are inferred to have evolved prior to oxygenation of the Earth’s atmosphere and now predominantly occur in anaerobes. Prevalent in both Chloroflexota and ca. Eulabeiota are capacities related to aerobic oxidation of gases, especially CO and H2. In fact, aerobic and anaerobic CO dehydrogenases are widespread throughout every class-level lineage, whereas traits such as denitrification and reductive dehalogenation are heterogeneously distributed across the supergroup. Interestingly, some Chloroflexota have a novel clade of group 3 NiFe hydrogenases that is phylogenetically distinct from previously reported groups. Overall, the analyses underline the very high level of metabolic diversity in the Chloroflexi supergroup, suggesting the ancestral metabolic platform for this group enabled highly varied adaptation to ecosystems that appeared in the aerobic world.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://figshare.com/projects/Chloroflexi_Supergroup/120267

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-ND 4.0 International license.
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Posted August 24, 2021.
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The Chloroflexi supergroup is metabolically diverse and representatives have novel genes for non-photosynthesis based CO2 fixation
Jacob A. West-Roberts, Paula B. Matheus-Carnevali, Marie Charlotte Schoelmerich, Basem Al-Shayeb, Alex D. Thomas, Allison Sharrar, Christine He, Lin-Xing Chen, Adi Lavy, Ray Keren, Yuki Amano, Jillian F. Banfield
bioRxiv 2021.08.23.457424; doi: https://doi.org/10.1101/2021.08.23.457424
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The Chloroflexi supergroup is metabolically diverse and representatives have novel genes for non-photosynthesis based CO2 fixation
Jacob A. West-Roberts, Paula B. Matheus-Carnevali, Marie Charlotte Schoelmerich, Basem Al-Shayeb, Alex D. Thomas, Allison Sharrar, Christine He, Lin-Xing Chen, Adi Lavy, Ray Keren, Yuki Amano, Jillian F. Banfield
bioRxiv 2021.08.23.457424; doi: https://doi.org/10.1101/2021.08.23.457424

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