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

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 εHao. 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 formore » 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.« less
Authors:
 [1] ;  [1] ;  [1] ;  [1] ;  [2] ;  [1] ;  [1] ;  [3] ;  [3] ;  [3] ;  [4] ;  [5] ;  [5] ;  [6] ;  [1] ;  [3] ;  [7] ;  [8] ;  [1]
  1. Russian Academy of Sciences, Moscow (Russia)
  2. Univ. of Queensland, St. Lucia, QLD (Australia)
  3. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  4. Newcastle Univ., Newcastle upon Tyne (United Kingdom)
  5. Leibniz Institute DSMZ - German Collection of Microorganisms and Cell Cultures, Braunschweig (Germany)
  6. Univ. of Pretoria, Pretoria (South Africa)
  7. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  8. Russian Academy of Sciences, Moscow (Russia); M.V. Lomonosov Moscow State Univ., Moscow (Russia); Skolkovo Institute of Science and Technology, Moscow (Russia); National Research Univ. - Higher School of Economics, Moscow (Russia)
Publication Date:
Grant/Contract Number:
AC02-05CH11231
Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 8; Journal Issue: FEB; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Research Org:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; bacterial evolution; phylogenomics; taxonomy; phylum; Caldithrix; genomic analysis; sequencing
OSTI Identifier:
1379740

Kublanov, Ilya V., Sigalova, Olga M., Gavrilov, Sergey N., Lebedinsky, Alexander V., Rinke, Christian, Kovaleva, Olga, Chernyh, Nikolai A., Ivanova, Natalia, Daum, Chris, Reddy, T. B. K., Klenk, Hans -Peter, Spring, Stefan, Goker, Markus, Reva, Oleg N., Miroshnichenko, Margarita L., Kyrpides, Nikos C., Woyke, Tanja, Gelfand, Mikhail S., and Bonch-Osmolovskaya, Elizaveta A.. Genomic Analysis of Caldithrix abyssi, the Thermophilic Anaerobic Bacterium of the Novel Bacterial Phylum Calditrichaeota. United States: N. p., Web. doi:10.3389/fmicb.2017.00195.
Kublanov, Ilya V., Sigalova, Olga M., Gavrilov, Sergey N., Lebedinsky, Alexander V., Rinke, Christian, Kovaleva, Olga, Chernyh, Nikolai A., Ivanova, Natalia, Daum, Chris, Reddy, T. B. K., Klenk, Hans -Peter, Spring, Stefan, Goker, Markus, Reva, Oleg N., Miroshnichenko, Margarita L., Kyrpides, Nikos C., Woyke, Tanja, Gelfand, Mikhail S., & Bonch-Osmolovskaya, Elizaveta A.. Genomic Analysis of Caldithrix abyssi, the Thermophilic Anaerobic Bacterium of the Novel Bacterial Phylum Calditrichaeota. United States. doi:10.3389/fmicb.2017.00195.
Kublanov, Ilya V., Sigalova, Olga M., Gavrilov, Sergey N., Lebedinsky, Alexander V., Rinke, Christian, Kovaleva, Olga, Chernyh, Nikolai A., Ivanova, Natalia, Daum, Chris, Reddy, T. B. K., Klenk, Hans -Peter, Spring, Stefan, Goker, Markus, Reva, Oleg N., Miroshnichenko, Margarita L., Kyrpides, Nikos C., Woyke, Tanja, Gelfand, Mikhail S., and Bonch-Osmolovskaya, Elizaveta A.. 2017. "Genomic Analysis of Caldithrix abyssi, the Thermophilic Anaerobic Bacterium of the Novel Bacterial Phylum Calditrichaeota". United States. doi:10.3389/fmicb.2017.00195. https://www.osti.gov/servlets/purl/1379740.
@article{osti_1379740,
title = {Genomic Analysis of Caldithrix abyssi, the Thermophilic Anaerobic Bacterium of the Novel Bacterial Phylum Calditrichaeota},
author = {Kublanov, Ilya V. and Sigalova, Olga M. and Gavrilov, Sergey N. and Lebedinsky, Alexander V. and Rinke, Christian and Kovaleva, Olga and Chernyh, Nikolai A. and Ivanova, Natalia and Daum, Chris and Reddy, T. B. K. and Klenk, Hans -Peter and Spring, Stefan and Goker, Markus and Reva, Oleg N. and Miroshnichenko, Margarita L. and Kyrpides, Nikos C. and Woyke, Tanja and Gelfand, Mikhail S. and Bonch-Osmolovskaya, Elizaveta A.},
abstractNote = {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 H2 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 εHao. 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 H2, 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.},
doi = {10.3389/fmicb.2017.00195},
journal = {Frontiers in Microbiology},
number = FEB,
volume = 8,
place = {United States},
year = {2017},
month = {2}
}

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