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Genomic Analysis of Caldithrix abyssi, the Thermophilic Anaerobic Bacterium of the Novel Bacterial Phylum Calditrichaeota

Lookup NU author(s): Professor Hans-Peter Klenk

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This work is licensed under a Creative Commons Attribution 4.0 International License (CC BY 4.0).


Abstract

The genome of Caldithrix abyssi, the first cultivated representative of a phylum-level bacterial lineage, was sequenced within the framework of Genomic Encyclopedia of Bacteria and Archaea (GEBA) project. The genomic analysis revealed mechanisms allowing this anaerobic bacterium to ferment peptides or to implement nitrate reduction with acetate or molecular hydrogen as electron donors. The genome encoded five different [NiFe]- and [FeFe]-hydrogenases, one of which, group 1 [NiFe]-hydrogenase, is presumably involved in lithoheterotrophic growth, three other produce H-2 during fermentation, and one is apparently bidirectional. The ability to reduce nitrate is determined by a nitrate reductase of the Nap family, while nitrite reduction to ammonia is presumably catalyzed by an octaheme cytochrome c nitrite reductase epsilon Hao. The genome contained genes of respiratory polysulfide/thiosulfate reductase, however, elemental sulfur and thiosulfate were not used as the electron acceptors for anaerobic respiration with acetate or H-2, probably due to the lack of the gene of the maturation protein. Nevertheless, elemental sulfur and thiosulfate stimulated growth on fermentable substrates (peptides), being reduced to sulfide, most probably through the action of the cytoplasmic sulfide dehydrogenase and/or NAD(P)-dependent [NiFe]-hydrogenase (sulfhydrogenase) encoded by the genome. Surprisingly, the genome of this anaerobic microorganism encoded all genes for cytochrome c oxidase, however, its maturation machinery seems to be non-operational due to genomic rearrangements of supplementary genes. Despite the fact that sugars were not among the substrates reported when C. abyssi was first described, our genomic analysis revealed multiple genes of glycoside hydrolases, and some of them were predicted to be secreted. This finding aided in bringing out four carbohydrates that supported the growth of C. abyssi: starch, cellobiose, glucomannan and xyloglucan. The genomic analysis demonstrated the ability of C. abyssi to synthesize nucleotides and most amino acids and vitamins. Finally, the genomic sequence allowed us to perform a phylogenomic analysis, based on 38 protein sequences, which confirmed the deep branching of this lineage and justified the proposal of a novel phylum Calditrichaeota.


Publication metadata

Author(s): Kublanov IV, Sigalova OM, Gavrilov SN, Lebedinsky AV, Rinke C, Kovaleva O, Chernyh NA, Ivanova N, Daum C, Reddy BK, Klenk HP, Spring S, Goker M, Reva ON, Miroshnichenko ML, Kyrpides NC, Woyke T, Gelfand MS, Bonch-Osmolovskaya EA

Publication type: Article

Publication status: Published

Journal: Frontiers in Microbiology

Year: 2017

Volume: 8

Online publication date: 20/02/2017

Acceptance date: 26/01/2017

Date deposited: 05/07/2017

ISSN (print): 1664-302X

Publisher: Frontiers Media SA

URL: http://doi.org/10.3389/fmicb.2017.00195

DOI: 10.3389/fmicb.2017.00195


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Funding

Funder referenceFunder name
14-04-00503Russian Foundation for Basic Research
14-24-00165RSF grant
14-24-00155Russian Science Foundation (RSF)
DE-AC02-05CH11231U.S. Department of Energy Joint Genome Institute, a DOE Office of Science User Facility

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