Comparative Genomics and Mutational Analysis Reveals a Novel XoxF-Utilizing Methylotroph in the Roseobacter Group Isolated From the Marine Environment

The Roseobacter group comprises a significant group of marine bacteria which are involved in global carbon and sulfur cycles. Some members are methylotrophs, using one-carbon compounds as a carbon and energy source. It has recently been shown that methylotrophs generally require a rare earth element...

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Main Authors: Alexandra M. Howat, John Vollmers, Martin Taubert, Carolina Grob, Joanna L. Dixon, Jonathan D. Todd, Yin Chen, Anne-Kristin Kaster, J. C. Murrell
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-04-01
Series:Frontiers in Microbiology
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fmicb.2018.00766/full
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spelling doaj-86e809bda3c7405d9d278562fb1074582020-11-24T22:27:30ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2018-04-01910.3389/fmicb.2018.00766370818Comparative Genomics and Mutational Analysis Reveals a Novel XoxF-Utilizing Methylotroph in the Roseobacter Group Isolated From the Marine EnvironmentAlexandra M. Howat0John Vollmers1Martin Taubert2Carolina Grob3Joanna L. Dixon4Jonathan D. Todd5Yin Chen6Anne-Kristin Kaster7J. C. Murrell8School of Environmental Sciences, University of East Anglia, Norwich, United KingdomInstitute for Biological Interfaces 5 (IBG-5), Karlsruhe Institute of Technology, Karlsruhe, GermanyAquatic Geomicrobiology, Institute of Biodiversity, Friedrich Schiller University Jena, Jena, GermanySchool of Environmental Sciences, University of East Anglia, Norwich, United KingdomPlymouth Marine Laboratory, Plymouth, United KingdomSchool of Biological Sciences, University of East Anglia, Norwich, United KingdomSchool of Life Sciences, University of Warwick, Coventry, United KingdomInstitute for Biological Interfaces 5 (IBG-5), Karlsruhe Institute of Technology, Karlsruhe, GermanySchool of Environmental Sciences, University of East Anglia, Norwich, United KingdomThe Roseobacter group comprises a significant group of marine bacteria which are involved in global carbon and sulfur cycles. Some members are methylotrophs, using one-carbon compounds as a carbon and energy source. It has recently been shown that methylotrophs generally require a rare earth element when using the methanol dehydrogenase enzyme XoxF for growth on methanol. Addition of lanthanum to methanol enrichments of coastal seawater facilitated the isolation of a novel methylotroph in the Roseobacter group: Marinibacterium anthonyi strain La 6. Mutation of xoxF5 revealed the essential nature of this gene during growth on methanol and ethanol. Physiological characterization demonstrated the metabolic versatility of this strain. Genome sequencing revealed that strain La 6 has the largest genome of all Roseobacter group members sequenced to date, at 7.18 Mbp. Multilocus sequence analysis (MLSA) showed that whilst it displays the highest core gene sequence similarity with subgroup 1 of the Roseobacter group, it shares very little of its pangenome, suggesting unique genetic adaptations. This research revealed that the addition of lanthanides to isolation procedures was key to cultivating novel XoxF-utilizing methylotrophs from the marine environment, whilst genome sequencing and MLSA provided insights into their potential genetic adaptations and relationship to the wider community.http://journal.frontiersin.org/article/10.3389/fmicb.2018.00766/fullmethylotrophyxoxFmarine environmentRoseobactercomparative genomicsmethanol
collection DOAJ
language English
format Article
sources DOAJ
author Alexandra M. Howat
John Vollmers
Martin Taubert
Carolina Grob
Joanna L. Dixon
Jonathan D. Todd
Yin Chen
Anne-Kristin Kaster
J. C. Murrell
spellingShingle Alexandra M. Howat
John Vollmers
Martin Taubert
Carolina Grob
Joanna L. Dixon
Jonathan D. Todd
Yin Chen
Anne-Kristin Kaster
J. C. Murrell
Comparative Genomics and Mutational Analysis Reveals a Novel XoxF-Utilizing Methylotroph in the Roseobacter Group Isolated From the Marine Environment
Frontiers in Microbiology
methylotrophy
xoxF
marine environment
Roseobacter
comparative genomics
methanol
author_facet Alexandra M. Howat
John Vollmers
Martin Taubert
Carolina Grob
Joanna L. Dixon
Jonathan D. Todd
Yin Chen
Anne-Kristin Kaster
J. C. Murrell
author_sort Alexandra M. Howat
title Comparative Genomics and Mutational Analysis Reveals a Novel XoxF-Utilizing Methylotroph in the Roseobacter Group Isolated From the Marine Environment
title_short Comparative Genomics and Mutational Analysis Reveals a Novel XoxF-Utilizing Methylotroph in the Roseobacter Group Isolated From the Marine Environment
title_full Comparative Genomics and Mutational Analysis Reveals a Novel XoxF-Utilizing Methylotroph in the Roseobacter Group Isolated From the Marine Environment
title_fullStr Comparative Genomics and Mutational Analysis Reveals a Novel XoxF-Utilizing Methylotroph in the Roseobacter Group Isolated From the Marine Environment
title_full_unstemmed Comparative Genomics and Mutational Analysis Reveals a Novel XoxF-Utilizing Methylotroph in the Roseobacter Group Isolated From the Marine Environment
title_sort comparative genomics and mutational analysis reveals a novel xoxf-utilizing methylotroph in the roseobacter group isolated from the marine environment
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2018-04-01
description The Roseobacter group comprises a significant group of marine bacteria which are involved in global carbon and sulfur cycles. Some members are methylotrophs, using one-carbon compounds as a carbon and energy source. It has recently been shown that methylotrophs generally require a rare earth element when using the methanol dehydrogenase enzyme XoxF for growth on methanol. Addition of lanthanum to methanol enrichments of coastal seawater facilitated the isolation of a novel methylotroph in the Roseobacter group: Marinibacterium anthonyi strain La 6. Mutation of xoxF5 revealed the essential nature of this gene during growth on methanol and ethanol. Physiological characterization demonstrated the metabolic versatility of this strain. Genome sequencing revealed that strain La 6 has the largest genome of all Roseobacter group members sequenced to date, at 7.18 Mbp. Multilocus sequence analysis (MLSA) showed that whilst it displays the highest core gene sequence similarity with subgroup 1 of the Roseobacter group, it shares very little of its pangenome, suggesting unique genetic adaptations. This research revealed that the addition of lanthanides to isolation procedures was key to cultivating novel XoxF-utilizing methylotrophs from the marine environment, whilst genome sequencing and MLSA provided insights into their potential genetic adaptations and relationship to the wider community.
topic methylotrophy
xoxF
marine environment
Roseobacter
comparative genomics
methanol
url http://journal.frontiersin.org/article/10.3389/fmicb.2018.00766/full
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