Cargando…

Expanding Characterized Diversity and the Pool of Complete Genome Sequences of Methylococcus Species, the Bacteria of High Environmental and Biotechnological Relevance

The bacterial genus Methylococcus, which comprises aerobic thermotolerant methanotrophic cocci, was described half-a-century ago. Over the years, a member of this genus, Methylococcus capsulatus Bath, has become a major model organism to study genomic and metabolic basis of obligate methanotrophy. H...

Descripción completa

Detalles Bibliográficos
Autores principales: Oshkin, Igor Y., Danilova, Olga V., But, Sergey Y., Miroshnikov, Kirill K., Suleimanov, Ruslan Z., Belova, Svetlana E., Tikhonova, Ekaterina N., Kuznetsov, Nikolai N., Khmelenina, Valentina N., Pimenov, Nikolai V., Dedysh, Svetlana N.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8527097/
https://www.ncbi.nlm.nih.gov/pubmed/34691008
http://dx.doi.org/10.3389/fmicb.2021.756830
_version_ 1784586011020361728
author Oshkin, Igor Y.
Danilova, Olga V.
But, Sergey Y.
Miroshnikov, Kirill K.
Suleimanov, Ruslan Z.
Belova, Svetlana E.
Tikhonova, Ekaterina N.
Kuznetsov, Nikolai N.
Khmelenina, Valentina N.
Pimenov, Nikolai V.
Dedysh, Svetlana N.
author_facet Oshkin, Igor Y.
Danilova, Olga V.
But, Sergey Y.
Miroshnikov, Kirill K.
Suleimanov, Ruslan Z.
Belova, Svetlana E.
Tikhonova, Ekaterina N.
Kuznetsov, Nikolai N.
Khmelenina, Valentina N.
Pimenov, Nikolai V.
Dedysh, Svetlana N.
author_sort Oshkin, Igor Y.
collection PubMed
description The bacterial genus Methylococcus, which comprises aerobic thermotolerant methanotrophic cocci, was described half-a-century ago. Over the years, a member of this genus, Methylococcus capsulatus Bath, has become a major model organism to study genomic and metabolic basis of obligate methanotrophy. High biotechnological potential of fast-growing Methylococcus species, mainly as a promising source of feed protein, has also been recognized. Despite this big research attention, the currently cultured Methylococcus diversity is represented by members of the two species, M. capsulatus and M. geothermalis, while finished genome sequences are available only for two strains of these methanotrophs. This study extends the pool of phenotypically characterized Methylococcus strains with good-quality genome sequences by contributing four novel isolates of these bacteria from activated sludge, landfill cover soil, and freshwater sediments. The determined genome sizes of novel isolates varied between 3.2 and 4.0Mb. As revealed by the phylogenomic analysis, strains IO1, BH, and KN2 affiliate with M. capsulatus, while strain Mc7 may potentially represent a novel species. Highest temperature optima (45–50°C) and highest growth rates in bioreactor cultures (up to 0.3h(−1)) were recorded for strains obtained from activated sludge. The comparative analysis of all complete genomes of Methylococcus species revealed 4,485 gene clusters. Of these, pan-genome core comprised 2,331 genes (on average 51.9% of each genome), with the accessory genome containing 846 and 1,308 genes in the shell and the cloud, respectively. Independently of the isolation source, all strains of M. capsulatus displayed surprisingly high genome synteny and a striking similarity in gene content. Strain Mc7 from a landfill cover soil differed from other isolates by the high content of mobile genetic elements in the genome and a number of genome-encoded features missing in M. capsulatus, such as sucrose biosynthesis and the ability to scavenge phosphorus and sulfur from the environment.
format Online
Article
Text
id pubmed-8527097
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-85270972021-10-21 Expanding Characterized Diversity and the Pool of Complete Genome Sequences of Methylococcus Species, the Bacteria of High Environmental and Biotechnological Relevance Oshkin, Igor Y. Danilova, Olga V. But, Sergey Y. Miroshnikov, Kirill K. Suleimanov, Ruslan Z. Belova, Svetlana E. Tikhonova, Ekaterina N. Kuznetsov, Nikolai N. Khmelenina, Valentina N. Pimenov, Nikolai V. Dedysh, Svetlana N. Front Microbiol Microbiology The bacterial genus Methylococcus, which comprises aerobic thermotolerant methanotrophic cocci, was described half-a-century ago. Over the years, a member of this genus, Methylococcus capsulatus Bath, has become a major model organism to study genomic and metabolic basis of obligate methanotrophy. High biotechnological potential of fast-growing Methylococcus species, mainly as a promising source of feed protein, has also been recognized. Despite this big research attention, the currently cultured Methylococcus diversity is represented by members of the two species, M. capsulatus and M. geothermalis, while finished genome sequences are available only for two strains of these methanotrophs. This study extends the pool of phenotypically characterized Methylococcus strains with good-quality genome sequences by contributing four novel isolates of these bacteria from activated sludge, landfill cover soil, and freshwater sediments. The determined genome sizes of novel isolates varied between 3.2 and 4.0Mb. As revealed by the phylogenomic analysis, strains IO1, BH, and KN2 affiliate with M. capsulatus, while strain Mc7 may potentially represent a novel species. Highest temperature optima (45–50°C) and highest growth rates in bioreactor cultures (up to 0.3h(−1)) were recorded for strains obtained from activated sludge. The comparative analysis of all complete genomes of Methylococcus species revealed 4,485 gene clusters. Of these, pan-genome core comprised 2,331 genes (on average 51.9% of each genome), with the accessory genome containing 846 and 1,308 genes in the shell and the cloud, respectively. Independently of the isolation source, all strains of M. capsulatus displayed surprisingly high genome synteny and a striking similarity in gene content. Strain Mc7 from a landfill cover soil differed from other isolates by the high content of mobile genetic elements in the genome and a number of genome-encoded features missing in M. capsulatus, such as sucrose biosynthesis and the ability to scavenge phosphorus and sulfur from the environment. Frontiers Media S.A. 2021-10-06 /pmc/articles/PMC8527097/ /pubmed/34691008 http://dx.doi.org/10.3389/fmicb.2021.756830 Text en Copyright © 2021 Oshkin, Danilova, But, Miroshnikov, Suleimanov, Belova, Tikhonova, Kuznetsov, Khmelenina, Pimenov and Dedysh. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Oshkin, Igor Y.
Danilova, Olga V.
But, Sergey Y.
Miroshnikov, Kirill K.
Suleimanov, Ruslan Z.
Belova, Svetlana E.
Tikhonova, Ekaterina N.
Kuznetsov, Nikolai N.
Khmelenina, Valentina N.
Pimenov, Nikolai V.
Dedysh, Svetlana N.
Expanding Characterized Diversity and the Pool of Complete Genome Sequences of Methylococcus Species, the Bacteria of High Environmental and Biotechnological Relevance
title Expanding Characterized Diversity and the Pool of Complete Genome Sequences of Methylococcus Species, the Bacteria of High Environmental and Biotechnological Relevance
title_full Expanding Characterized Diversity and the Pool of Complete Genome Sequences of Methylococcus Species, the Bacteria of High Environmental and Biotechnological Relevance
title_fullStr Expanding Characterized Diversity and the Pool of Complete Genome Sequences of Methylococcus Species, the Bacteria of High Environmental and Biotechnological Relevance
title_full_unstemmed Expanding Characterized Diversity and the Pool of Complete Genome Sequences of Methylococcus Species, the Bacteria of High Environmental and Biotechnological Relevance
title_short Expanding Characterized Diversity and the Pool of Complete Genome Sequences of Methylococcus Species, the Bacteria of High Environmental and Biotechnological Relevance
title_sort expanding characterized diversity and the pool of complete genome sequences of methylococcus species, the bacteria of high environmental and biotechnological relevance
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8527097/
https://www.ncbi.nlm.nih.gov/pubmed/34691008
http://dx.doi.org/10.3389/fmicb.2021.756830
work_keys_str_mv AT oshkinigory expandingcharacterizeddiversityandthepoolofcompletegenomesequencesofmethylococcusspeciesthebacteriaofhighenvironmentalandbiotechnologicalrelevance
AT danilovaolgav expandingcharacterizeddiversityandthepoolofcompletegenomesequencesofmethylococcusspeciesthebacteriaofhighenvironmentalandbiotechnologicalrelevance
AT butsergeyy expandingcharacterizeddiversityandthepoolofcompletegenomesequencesofmethylococcusspeciesthebacteriaofhighenvironmentalandbiotechnologicalrelevance
AT miroshnikovkirillk expandingcharacterizeddiversityandthepoolofcompletegenomesequencesofmethylococcusspeciesthebacteriaofhighenvironmentalandbiotechnologicalrelevance
AT suleimanovruslanz expandingcharacterizeddiversityandthepoolofcompletegenomesequencesofmethylococcusspeciesthebacteriaofhighenvironmentalandbiotechnologicalrelevance
AT belovasvetlanae expandingcharacterizeddiversityandthepoolofcompletegenomesequencesofmethylococcusspeciesthebacteriaofhighenvironmentalandbiotechnologicalrelevance
AT tikhonovaekaterinan expandingcharacterizeddiversityandthepoolofcompletegenomesequencesofmethylococcusspeciesthebacteriaofhighenvironmentalandbiotechnologicalrelevance
AT kuznetsovnikolain expandingcharacterizeddiversityandthepoolofcompletegenomesequencesofmethylococcusspeciesthebacteriaofhighenvironmentalandbiotechnologicalrelevance
AT khmeleninavalentinan expandingcharacterizeddiversityandthepoolofcompletegenomesequencesofmethylococcusspeciesthebacteriaofhighenvironmentalandbiotechnologicalrelevance
AT pimenovnikolaiv expandingcharacterizeddiversityandthepoolofcompletegenomesequencesofmethylococcusspeciesthebacteriaofhighenvironmentalandbiotechnologicalrelevance
AT dedyshsvetlanan expandingcharacterizeddiversityandthepoolofcompletegenomesequencesofmethylococcusspeciesthebacteriaofhighenvironmentalandbiotechnologicalrelevance