Saccharibacteria harness light energy using type-1 rhodopsins that may rely on retinal sourced from microbial hosts
Open accessPublished version of a preprint
Abstract
Microbial rhodopsins are a family of photoreceptive membrane proteins with a wide distribution across the Tree of Life. Within the candidate phyla radiation (CPR), a diverse group of putatively episymbiotic bacteria, the genetic potential to produce rhodopsins appears to be confined to a small clade of organisms from sunlit environments. Here, we characterize the metabolic context and biophysical features of Saccharibacteria Type-1 rhodopsin sequences derived from metagenomic surveys and show that these proteins function as outward proton pumps. This provides one of the only known mechanisms by which CPR can generate a proton gradient for ATP synthesis. These Saccharibacteria do not encode the genetic machinery to produce all-trans-retinal, the chromophore essential for rhodopsin function, but their rhodopsins are able to rapidly uptake this cofactor when provided in experimental assays. We found consistent evidence for the capacity to produce retinal from β-carotene in microorganisms co-occurring with Saccharibacteria, and this genetic potential was dominated by members of the Actinobacteria, which are known hosts of Saccharibacteria in other habitats. If Actinobacteria serve as hosts for Saccharibacteria in freshwater environments, exchange of retinal for use by rhodopsin may be a feature of their associations.
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Cites
Highly accurate protein structure prediction with AlphaFold
Jumper, J., Evans, R., Pritzel, A., Green, T., Figurnov, M., Ronneberger, O., Tunyasuvunakool, K., Bates, R., Žídek, A., Potapenko, A., et al. (2021) · Nature · doi:10.1038/s41586-021-03819-2 · Cited by 43,764 · see citing works
ColabFold - Making protein folding accessible to all
Mirdita, M., Schütze, K., Moriwaki, Y., Heo, L., Ovchinnikov, S., & Steinegger, M. (2021) · doi:10.1101/2021.08.15.456425 · Cited by 9,391 · see citing works
Unusual biology across a group comprising more than 15% of domain Bacteria
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“Only recently was it suggested that some members of the candidate phyla radiation (CPR)—a highly diverse group of bacteria originally detected by 16 S rRNA sequencing [1] and subsequently characterized by genomeresolved metagenomics [2, 3]—may be able to use rhodopsins for proton translocation and thus energy generati…”
BackgroundSelf-citationLevy Karin, E., Mirdita, M., & Söding, J. (2020) · Microbiome · doi:10.1186/s40168-020-00808-x · Cited by 299 · see citing works
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- Authors
- Jaffe, A. L., Konno, M., Kawasaki, Y., Kataoka, C., Béjà, O., Kandori, H., Inoue, K., & Banfield, J. F.
- Affiliations
- University of California, Berkeley (US)
- Japan Science and Technology Agency (JP)
- The Institute for Solid State Physics, The University of Tokyo (JP)
- Nagoya Institute of Technology (JP)
- Technion – Israel Institute of Technology (IL)
- Innovative Genomics Institute (US)
- Corresponding author
- Inoue, Keiichi
- Banfield, Jillian F
- ORCID
- Venue
- The ISME Journal
- Publisher
- Oxford University Press (OUP)
- Published
- 2022-04-19
- Volume
- 16
- Issue
- 8
- Pages
- 2056-2059
- ISSN
- 1751-7362 (ISSN-L)
- 1751-7370
- PMC
- PMC9296517
- OpenAlex
- W4226136129
- Cited by
- 32
- References
- 4
- Citations by year
- 2025: 7 · 2024: 12 · 2023: 8 · 2022: 4
- FWCI
- 4.20
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- The ISME Journal (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion, cc-by)
- Funders
- Gordon and Betty Moore Foundation (Grant 71785, 71785)
- Innovative Genomics Institute
- Ministry of Education, Culture, Sports, Science and Technology (JP21H01875, JP20H05758)
- Japan Society for the Promotion of Science (20K21383, 23K21092, JP20H05758, 21H04969, JP21H01875, 20H05758)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Photoreceptor and optogenetics research
- Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- Saccharibacteria, microbial rhodopsins, Candidate Phyla Radiation, all-trans-retinal, beta-carotene, actinobacteria, host-symbiont association, proton pump, light energy harvesting, photosynthetic bacteria, ATP production, metagenomics
- MeSH terms
- Bacteria, Light, Rhodopsin, Proton Pumps, Rhodopsins, Microbial, Actinobacteria
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