Zetaproteobacteria Pan-Genome Reveals Candidate Gene Cluster for Twisted Stalk Biosynthesis and Export
Twisted stalks are morphologically unique bacterial extracellular organo-metallic structures containing Fe(III) oxyhydroxides that are produced by microaerophilic Fe(II)-oxidizers belonging to the Betaproteobacteria and Zetaproteobacteria. Understanding the underlying genetic and physiological mecha...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2021-06-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2021.679409/full |
| _version_ | 1818602766045544448 |
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| author | Elif Koeksoy Elif Koeksoy Oliver M. Bezuidt Timm Bayer Clara S. Chan Clara S. Chan David Emerson |
| author_facet | Elif Koeksoy Elif Koeksoy Oliver M. Bezuidt Timm Bayer Clara S. Chan Clara S. Chan David Emerson |
| author_sort | Elif Koeksoy |
| collection | DOAJ |
| description | Twisted stalks are morphologically unique bacterial extracellular organo-metallic structures containing Fe(III) oxyhydroxides that are produced by microaerophilic Fe(II)-oxidizers belonging to the Betaproteobacteria and Zetaproteobacteria. Understanding the underlying genetic and physiological mechanisms of stalk formation is of great interest based on their potential as novel biogenic nanomaterials and their relevance as putative biomarkers for microbial Fe(II) oxidation on ancient Earth. Despite the recognition of these special biominerals for over 150 years, the genetic foundation for the stalk phenotype has remained unresolved. Here we present a candidate gene cluster for the biosynthesis and secretion of the stalk organic matrix that we identified with a trait-based analyses of a pan-genome comprising 16 Zetaproteobacteria isolate genomes. The “stalk formation in Zetaproteobacteria” (sfz) cluster comprises six genes (sfz1-sfz6), of which sfz1 and sfz2 were predicted with functions in exopolysaccharide synthesis, regulation, and export, sfz4 and sfz6 with functions in cell wall synthesis manipulation and carbohydrate hydrolysis, and sfz3 and sfz5 with unknown functions. The stalk-forming Betaproteobacteria Ferriphaselus R-1 and OYT-1, as well as dread-forming Zetaproteobacteria Mariprofundus aestuarium CP-5 and Mariprofundus ferrinatatus CP-8 contain distant sfz gene homologs, whereas stalk-less Zetaproteobacteria and Betaproteobacteria lack the entire gene cluster. Our pan-genome analysis further revealed a significant enrichment of clusters of orthologous groups (COGs) across all Zetaproteobacteria isolate genomes that are associated with the regulation of a switch between sessile and motile growth controlled by the intracellular signaling molecule c-di-GMP. Potential interactions between stalk-former unique transcription factor genes, sfz genes, and c-di-GMP point toward a c-di-GMP regulated surface attachment function of stalks during sessile growth. |
| first_indexed | 2024-12-16T13:12:29Z |
| format | Article |
| id | doaj.art-9324ecc06d2541fe9c5758fdf12dd3ba |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-16T13:12:29Z |
| publishDate | 2021-06-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-9324ecc06d2541fe9c5758fdf12dd3ba2022-12-21T22:30:34ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-06-011210.3389/fmicb.2021.679409679409Zetaproteobacteria Pan-Genome Reveals Candidate Gene Cluster for Twisted Stalk Biosynthesis and ExportElif Koeksoy0Elif Koeksoy1Oliver M. Bezuidt2Timm Bayer3Clara S. Chan4Clara S. Chan5David Emerson6Bigelow Laboratory for Ocean Sciences, East Boothbay, ME, United StatesLeibniz Institute DSMZ (German Collection of Microorganisms and Cell Cultures), Braunschweig, GermanyBigelow Laboratory for Ocean Sciences, East Boothbay, ME, United StatesGeomicrobiology Group, Center for Applied Geoscience, University of Tübingen, Tübingen, GermanyDepartment of Earth Sciences, University of Delaware, Newark, DE, United StatesSchool of Marine Sciences and Policy, University of Delaware, Newark, DE, United StatesBigelow Laboratory for Ocean Sciences, East Boothbay, ME, United StatesTwisted stalks are morphologically unique bacterial extracellular organo-metallic structures containing Fe(III) oxyhydroxides that are produced by microaerophilic Fe(II)-oxidizers belonging to the Betaproteobacteria and Zetaproteobacteria. Understanding the underlying genetic and physiological mechanisms of stalk formation is of great interest based on their potential as novel biogenic nanomaterials and their relevance as putative biomarkers for microbial Fe(II) oxidation on ancient Earth. Despite the recognition of these special biominerals for over 150 years, the genetic foundation for the stalk phenotype has remained unresolved. Here we present a candidate gene cluster for the biosynthesis and secretion of the stalk organic matrix that we identified with a trait-based analyses of a pan-genome comprising 16 Zetaproteobacteria isolate genomes. The “stalk formation in Zetaproteobacteria” (sfz) cluster comprises six genes (sfz1-sfz6), of which sfz1 and sfz2 were predicted with functions in exopolysaccharide synthesis, regulation, and export, sfz4 and sfz6 with functions in cell wall synthesis manipulation and carbohydrate hydrolysis, and sfz3 and sfz5 with unknown functions. The stalk-forming Betaproteobacteria Ferriphaselus R-1 and OYT-1, as well as dread-forming Zetaproteobacteria Mariprofundus aestuarium CP-5 and Mariprofundus ferrinatatus CP-8 contain distant sfz gene homologs, whereas stalk-less Zetaproteobacteria and Betaproteobacteria lack the entire gene cluster. Our pan-genome analysis further revealed a significant enrichment of clusters of orthologous groups (COGs) across all Zetaproteobacteria isolate genomes that are associated with the regulation of a switch between sessile and motile growth controlled by the intracellular signaling molecule c-di-GMP. Potential interactions between stalk-former unique transcription factor genes, sfz genes, and c-di-GMP point toward a c-di-GMP regulated surface attachment function of stalks during sessile growth.https://www.frontiersin.org/articles/10.3389/fmicb.2021.679409/fullzetaproteobacteriaFe-biosignaturesbiomineralizationtwisted stalkspan-genomemicroaerophilic Fe(II) oxidation |
| spellingShingle | Elif Koeksoy Elif Koeksoy Oliver M. Bezuidt Timm Bayer Clara S. Chan Clara S. Chan David Emerson Zetaproteobacteria Pan-Genome Reveals Candidate Gene Cluster for Twisted Stalk Biosynthesis and Export Frontiers in Microbiology zetaproteobacteria Fe-biosignatures biomineralization twisted stalks pan-genome microaerophilic Fe(II) oxidation |
| title | Zetaproteobacteria Pan-Genome Reveals Candidate Gene Cluster for Twisted Stalk Biosynthesis and Export |
| title_full | Zetaproteobacteria Pan-Genome Reveals Candidate Gene Cluster for Twisted Stalk Biosynthesis and Export |
| title_fullStr | Zetaproteobacteria Pan-Genome Reveals Candidate Gene Cluster for Twisted Stalk Biosynthesis and Export |
| title_full_unstemmed | Zetaproteobacteria Pan-Genome Reveals Candidate Gene Cluster for Twisted Stalk Biosynthesis and Export |
| title_short | Zetaproteobacteria Pan-Genome Reveals Candidate Gene Cluster for Twisted Stalk Biosynthesis and Export |
| title_sort | zetaproteobacteria pan genome reveals candidate gene cluster for twisted stalk biosynthesis and export |
| topic | zetaproteobacteria Fe-biosignatures biomineralization twisted stalks pan-genome microaerophilic Fe(II) oxidation |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2021.679409/full |
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