Horizontal acquisition of hydrogen conversion ability and other habitat adaptations in the Hydrogenovibrio strains SP-41 and XCL-2

Abstract Background Obligate sulfur oxidizing chemolithoauthotrophic strains of Hydrogenovibrio crunogenus have been isolated from multiple hydrothermal vent associated habitats. However, a hydrogenase gene cluster (encoding the hydrogen converting enzyme and its maturation/assembly machinery) detec...

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Main Authors: Giorgio Gonnella, Nicole Adam, Mirjam Perner
Format: Article
Language:English
Published: BMC 2019-05-01
Series:BMC Genomics
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12864-019-5710-5
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spelling doaj-df73c9ba9fe342e1a38a87b76070ff682020-11-25T02:58:54ZengBMCBMC Genomics1471-21642019-05-0120111910.1186/s12864-019-5710-5Horizontal acquisition of hydrogen conversion ability and other habitat adaptations in the Hydrogenovibrio strains SP-41 and XCL-2Giorgio Gonnella0Nicole Adam1Mirjam Perner2Universität Hamburg, MIN-Fakultät, ZBH - Center for BioinformaticsGEOMAR Helmholtz Center for Ocean Research Kiel, GeomicrobiologyGEOMAR Helmholtz Center for Ocean Research Kiel, GeomicrobiologyAbstract Background Obligate sulfur oxidizing chemolithoauthotrophic strains of Hydrogenovibrio crunogenus have been isolated from multiple hydrothermal vent associated habitats. However, a hydrogenase gene cluster (encoding the hydrogen converting enzyme and its maturation/assembly machinery) detected on the first sequenced H. crunogenus strain (XCL-2) suggested that hydrogen conversion may also play a role in this organism. Yet, numerous experiments have underlined XCL-2’s inability to consume hydrogen under the tested conditions. A recent study showed that the closely related strain SP-41 contains a homolog of the XCL-2 hydrogenase (a group 1b [NiFe]-hydrogenase), but that it can indeed use hydrogen. Hence, the question remained unresolved, why SP-41 is capable of using hydrogen, while XCL-2 is not. Results Here, we present the genome sequence of the SP-41 strain and compare it to that of the XCL-2 strain. We show that the chromosome of SP-41 codes for a further hydrogenase gene cluster, including two additional hydrogenases: the first appears to be a group 1d periplasmic membrane-anchored hydrogenase, and the second a group 2b sensory hydrogenase. The region where these genes are located was likely acquired horizontally and exhibits similarity to other Hydrogenovibrio species (H. thermophilus MA2-6 and H. marinus MH-110 T ) and other hydrogen oxidizing Proteobacteria (Cupriavidus necator H16 and Ghiorsea bivora TAG-1 T ). The genomes of XCL-2 and SP-41 show a strong conservation in gene order. However, several short genomic regions are not contained in the genome of the other strain. These exclusive regions are often associated with signs of DNA mobility, such as genes coding for transposases. They code for transport systems and/or extend the metabolic potential of the strains. Conclusions Our results suggest that horizontal gene transfer plays an important role in shaping the genomes of these strains, as a likely mechanism for habitat adaptation, including, but not limited to the transfer of the hydrogen conversion ability.http://link.springer.com/article/10.1186/s12864-019-5710-5HydrogenaseHydrogenovibrioHorizontal gene transferHydrothermal ventsHabitat adaptationBacterial genome
collection DOAJ
language English
format Article
sources DOAJ
author Giorgio Gonnella
Nicole Adam
Mirjam Perner
spellingShingle Giorgio Gonnella
Nicole Adam
Mirjam Perner
Horizontal acquisition of hydrogen conversion ability and other habitat adaptations in the Hydrogenovibrio strains SP-41 and XCL-2
BMC Genomics
Hydrogenase
Hydrogenovibrio
Horizontal gene transfer
Hydrothermal vents
Habitat adaptation
Bacterial genome
author_facet Giorgio Gonnella
Nicole Adam
Mirjam Perner
author_sort Giorgio Gonnella
title Horizontal acquisition of hydrogen conversion ability and other habitat adaptations in the Hydrogenovibrio strains SP-41 and XCL-2
title_short Horizontal acquisition of hydrogen conversion ability and other habitat adaptations in the Hydrogenovibrio strains SP-41 and XCL-2
title_full Horizontal acquisition of hydrogen conversion ability and other habitat adaptations in the Hydrogenovibrio strains SP-41 and XCL-2
title_fullStr Horizontal acquisition of hydrogen conversion ability and other habitat adaptations in the Hydrogenovibrio strains SP-41 and XCL-2
title_full_unstemmed Horizontal acquisition of hydrogen conversion ability and other habitat adaptations in the Hydrogenovibrio strains SP-41 and XCL-2
title_sort horizontal acquisition of hydrogen conversion ability and other habitat adaptations in the hydrogenovibrio strains sp-41 and xcl-2
publisher BMC
series BMC Genomics
issn 1471-2164
publishDate 2019-05-01
description Abstract Background Obligate sulfur oxidizing chemolithoauthotrophic strains of Hydrogenovibrio crunogenus have been isolated from multiple hydrothermal vent associated habitats. However, a hydrogenase gene cluster (encoding the hydrogen converting enzyme and its maturation/assembly machinery) detected on the first sequenced H. crunogenus strain (XCL-2) suggested that hydrogen conversion may also play a role in this organism. Yet, numerous experiments have underlined XCL-2’s inability to consume hydrogen under the tested conditions. A recent study showed that the closely related strain SP-41 contains a homolog of the XCL-2 hydrogenase (a group 1b [NiFe]-hydrogenase), but that it can indeed use hydrogen. Hence, the question remained unresolved, why SP-41 is capable of using hydrogen, while XCL-2 is not. Results Here, we present the genome sequence of the SP-41 strain and compare it to that of the XCL-2 strain. We show that the chromosome of SP-41 codes for a further hydrogenase gene cluster, including two additional hydrogenases: the first appears to be a group 1d periplasmic membrane-anchored hydrogenase, and the second a group 2b sensory hydrogenase. The region where these genes are located was likely acquired horizontally and exhibits similarity to other Hydrogenovibrio species (H. thermophilus MA2-6 and H. marinus MH-110 T ) and other hydrogen oxidizing Proteobacteria (Cupriavidus necator H16 and Ghiorsea bivora TAG-1 T ). The genomes of XCL-2 and SP-41 show a strong conservation in gene order. However, several short genomic regions are not contained in the genome of the other strain. These exclusive regions are often associated with signs of DNA mobility, such as genes coding for transposases. They code for transport systems and/or extend the metabolic potential of the strains. Conclusions Our results suggest that horizontal gene transfer plays an important role in shaping the genomes of these strains, as a likely mechanism for habitat adaptation, including, but not limited to the transfer of the hydrogen conversion ability.
topic Hydrogenase
Hydrogenovibrio
Horizontal gene transfer
Hydrothermal vents
Habitat adaptation
Bacterial genome
url http://link.springer.com/article/10.1186/s12864-019-5710-5
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