Comparative Metabolomics of <named-content content-type="genus-species">Mycoplasma bovis</named-content> and <named-content content-type="genus-species">Mycoplasma gallisepticum</named-content> Reveals Fundamental Differences in Active Metabolic Pathways and Suggests Novel Gene Annotations

ABSTRACT Mycoplasmas are simple, but successful parasites that have the smallest genome of any free-living cell and are thought to have a highly streamlined cellular metabolism. Here, we have undertaken a detailed metabolomic analysis of two species, Mycoplasma bovis and Mycoplasma gallisepticum, wh...

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Autores principales:	Y. Masukagami, D. P. De Souza, S. Dayalan, C. Bowen, S. O’Callaghan, K. Kouremenos, B. Nijagal, D. Tull, K. A. Tivendale, P. F. Markham, M. J. McConville, G. F. Browning, F. M. Sansom
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	carbon metabolism genome annotation metabolomics mycoplasma Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/76623dac46f24ccba9bfe1cd522370e4
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spelling	oai:doaj.org-article:76623dac46f24ccba9bfe1cd522370e42021-12-02T18:15:43ZComparative Metabolomics of <named-content content-type="genus-species">Mycoplasma bovis</named-content> and <named-content content-type="genus-species">Mycoplasma gallisepticum</named-content> Reveals Fundamental Differences in Active Metabolic Pathways and Suggests Novel Gene Annotations10.1128/mSystems.00055-172379-5077https://doaj.org/article/76623dac46f24ccba9bfe1cd522370e42017-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00055-17https://doaj.org/toc/2379-5077ABSTRACT Mycoplasmas are simple, but successful parasites that have the smallest genome of any free-living cell and are thought to have a highly streamlined cellular metabolism. Here, we have undertaken a detailed metabolomic analysis of two species, Mycoplasma bovis and Mycoplasma gallisepticum, which cause economically important diseases in cattle and poultry, respectively. Untargeted gas chromatography-mass spectrometry and liquid chromatography-mass spectrometry analyses of mycoplasma metabolite extracts revealed significant differences in the steady-state levels of many metabolites in central carbon metabolism, while 13C stable isotope labeling studies revealed marked differences in carbon source utilization. These data were mapped onto in silico metabolic networks predicted from genome wide annotations. The analyses elucidated distinct differences, including a clear difference in glucose utilization, with a marked decrease in glucose uptake and glycolysis in M. bovis compared to M. gallisepticum, which may reflect differing host nutrient availabilities. The 13C-labeling patterns also revealed several functional metabolic pathways that were previously unannotated in these species, allowing us to assign putative enzyme functions to the products of a number of genes of unknown function, especially in M. bovis. This study demonstrates the considerable potential of metabolomic analyses to assist in characterizing significant differences in the metabolism of different bacterial species and in improving genome annotation. IMPORTANCE Mycoplasmas are pathogenic bacteria that cause serious chronic infections in production animals, resulting in considerable losses worldwide, as well as causing disease in humans. These bacteria have extremely reduced genomes and are thought to have limited metabolic flexibility, even though they are highly successful persistent parasites in a diverse number of species. The extent to which different Mycoplasma species are capable of catabolizing host carbon sources and nutrients, or synthesizing essential metabolites, remains poorly defined. We have used advanced metabolomic techniques to identify metabolic pathways that are active in two species of Mycoplasma that infect distinct hosts (poultry and cattle). We show that these species exhibit marked differences in metabolite steady-state levels and carbon source utilization. This information has been used to functionally characterize previously unknown genes in the genomes of these pathogens. These species-specific differences are likely to reflect important differences in host nutrient levels and pathogenic mechanisms.Y. MasukagamiD. P. De SouzaS. DayalanC. BowenS. O’CallaghanK. KouremenosB. NijagalD. TullK. A. TivendaleP. F. MarkhamM. J. McConvilleG. F. BrowningF. M. SansomAmerican Society for Microbiologyarticlecarbon metabolismgenome annotationmetabolomicsmycoplasmaMicrobiologyQR1-502ENmSystems, Vol 2, Iss 5 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	carbon metabolism genome annotation metabolomics mycoplasma Microbiology QR1-502
spellingShingle	carbon metabolism genome annotation metabolomics mycoplasma Microbiology QR1-502 Y. Masukagami D. P. De Souza S. Dayalan C. Bowen S. O’Callaghan K. Kouremenos B. Nijagal D. Tull K. A. Tivendale P. F. Markham M. J. McConville G. F. Browning F. M. Sansom Comparative Metabolomics of <named-content content-type="genus-species">Mycoplasma bovis</named-content> and <named-content content-type="genus-species">Mycoplasma gallisepticum</named-content> Reveals Fundamental Differences in Active Metabolic Pathways and Suggests Novel Gene Annotations
description	ABSTRACT Mycoplasmas are simple, but successful parasites that have the smallest genome of any free-living cell and are thought to have a highly streamlined cellular metabolism. Here, we have undertaken a detailed metabolomic analysis of two species, Mycoplasma bovis and Mycoplasma gallisepticum, which cause economically important diseases in cattle and poultry, respectively. Untargeted gas chromatography-mass spectrometry and liquid chromatography-mass spectrometry analyses of mycoplasma metabolite extracts revealed significant differences in the steady-state levels of many metabolites in central carbon metabolism, while 13C stable isotope labeling studies revealed marked differences in carbon source utilization. These data were mapped onto in silico metabolic networks predicted from genome wide annotations. The analyses elucidated distinct differences, including a clear difference in glucose utilization, with a marked decrease in glucose uptake and glycolysis in M. bovis compared to M. gallisepticum, which may reflect differing host nutrient availabilities. The 13C-labeling patterns also revealed several functional metabolic pathways that were previously unannotated in these species, allowing us to assign putative enzyme functions to the products of a number of genes of unknown function, especially in M. bovis. This study demonstrates the considerable potential of metabolomic analyses to assist in characterizing significant differences in the metabolism of different bacterial species and in improving genome annotation. IMPORTANCE Mycoplasmas are pathogenic bacteria that cause serious chronic infections in production animals, resulting in considerable losses worldwide, as well as causing disease in humans. These bacteria have extremely reduced genomes and are thought to have limited metabolic flexibility, even though they are highly successful persistent parasites in a diverse number of species. The extent to which different Mycoplasma species are capable of catabolizing host carbon sources and nutrients, or synthesizing essential metabolites, remains poorly defined. We have used advanced metabolomic techniques to identify metabolic pathways that are active in two species of Mycoplasma that infect distinct hosts (poultry and cattle). We show that these species exhibit marked differences in metabolite steady-state levels and carbon source utilization. This information has been used to functionally characterize previously unknown genes in the genomes of these pathogens. These species-specific differences are likely to reflect important differences in host nutrient levels and pathogenic mechanisms.
format	article
author	Y. Masukagami D. P. De Souza S. Dayalan C. Bowen S. O’Callaghan K. Kouremenos B. Nijagal D. Tull K. A. Tivendale P. F. Markham M. J. McConville G. F. Browning F. M. Sansom
author_facet	Y. Masukagami D. P. De Souza S. Dayalan C. Bowen S. O’Callaghan K. Kouremenos B. Nijagal D. Tull K. A. Tivendale P. F. Markham M. J. McConville G. F. Browning F. M. Sansom
author_sort	Y. Masukagami
title	Comparative Metabolomics of <named-content content-type="genus-species">Mycoplasma bovis</named-content> and <named-content content-type="genus-species">Mycoplasma gallisepticum</named-content> Reveals Fundamental Differences in Active Metabolic Pathways and Suggests Novel Gene Annotations
title_short	Comparative Metabolomics of <named-content content-type="genus-species">Mycoplasma bovis</named-content> and <named-content content-type="genus-species">Mycoplasma gallisepticum</named-content> Reveals Fundamental Differences in Active Metabolic Pathways and Suggests Novel Gene Annotations
title_full	Comparative Metabolomics of <named-content content-type="genus-species">Mycoplasma bovis</named-content> and <named-content content-type="genus-species">Mycoplasma gallisepticum</named-content> Reveals Fundamental Differences in Active Metabolic Pathways and Suggests Novel Gene Annotations
title_fullStr	Comparative Metabolomics of <named-content content-type="genus-species">Mycoplasma bovis</named-content> and <named-content content-type="genus-species">Mycoplasma gallisepticum</named-content> Reveals Fundamental Differences in Active Metabolic Pathways and Suggests Novel Gene Annotations
title_full_unstemmed	Comparative Metabolomics of <named-content content-type="genus-species">Mycoplasma bovis</named-content> and <named-content content-type="genus-species">Mycoplasma gallisepticum</named-content> Reveals Fundamental Differences in Active Metabolic Pathways and Suggests Novel Gene Annotations
title_sort	comparative metabolomics of <named-content content-type="genus-species">mycoplasma bovis</named-content> and <named-content content-type="genus-species">mycoplasma gallisepticum</named-content> reveals fundamental differences in active metabolic pathways and suggests novel gene annotations
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/76623dac46f24ccba9bfe1cd522370e4
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Comparative Metabolomics of <named-content content-type="genus-species">Mycoplasma bovis</named-content> and <named-content content-type="genus-species">Mycoplasma gallisepticum</named-content> Reveals Fundamental Differences in Active Metabolic Pathways and Suggests Novel Gene Annotations

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