Key Transitions in the Evolution of Rapid and Slow Growing Mycobacteria Identified by Comparative Genomics
Mycobacteria have been classified into rapid and slow growing phenotypes, but the genetic factors that underlie these growth rate differences are not well understood. We compared the genomes of 157 mycobacterial species, representing all major branches of the mycobacterial phylogenetic tree to ident...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2020-01-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2019.03019/full |
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| author | Nathan L. Bachmann Nathan L. Bachmann Rauf Salamzade Abigail L. Manson Richard Whittington Richard Whittington Vitali Sintchenko Vitali Sintchenko Ashlee M. Earl Ben J. Marais |
| author_facet | Nathan L. Bachmann Nathan L. Bachmann Rauf Salamzade Abigail L. Manson Richard Whittington Richard Whittington Vitali Sintchenko Vitali Sintchenko Ashlee M. Earl Ben J. Marais |
| author_sort | Nathan L. Bachmann |
| collection | DOAJ |
| description | Mycobacteria have been classified into rapid and slow growing phenotypes, but the genetic factors that underlie these growth rate differences are not well understood. We compared the genomes of 157 mycobacterial species, representing all major branches of the mycobacterial phylogenetic tree to identify genes and operons enriched among rapid and slow growing mycobacteria. Overlaying growth phenotype on a phylogenetic tree based on 304 core genes suggested that ancestral mycobacteria had a rapid growth phenotype with a single major evolutionary separation into rapid and slow growing sub-genera. We identified 293 genes enriched among rapid growing sub-genera, including genes encoding for amino acid transport/metabolism (e.g., livFGMH operon) and transcription, as well as novel ABC transporters. Loss of the livFGMH and ABC transporter operons among slow growing species suggests that reduced cellular amino acid transport may be growth limiting. Comparative genomic analysis suggests that horizontal gene transfer, from non-mycobacterial genera, may have contributed to niche adaptation and pathogenicity, especially among slow growing species. Interestingly, the mammalian cell entry (mce) operon was found to be ubiquitous, irrespective of growth phenotype or pathogenicity, although protein sequence homology between rapid and slow growing species was low (<50%). This suggests that the mce operon was present in ancestral rapid growing species, but later adapted by slow growing species for use as a mechanism to establish an intra-cellular lifestyle. |
| first_indexed | 2024-12-21T22:46:57Z |
| format | Article |
| id | doaj.art-2d02609c911a43a9abc3a7a206f307be |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-21T22:46:57Z |
| publishDate | 2020-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-2d02609c911a43a9abc3a7a206f307be2022-12-21T18:47:41ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-01-011010.3389/fmicb.2019.03019495775Key Transitions in the Evolution of Rapid and Slow Growing Mycobacteria Identified by Comparative GenomicsNathan L. Bachmann0Nathan L. Bachmann1Rauf Salamzade2Abigail L. Manson3Richard Whittington4Richard Whittington5Vitali Sintchenko6Vitali Sintchenko7Ashlee M. Earl8Ben J. Marais9NSW Mycobacterium Reference Laboratory, Centre for Infectious Diseases and Microbiology Laboratory Services, Institute of Clinical Pathology and Medical Research – Pathology West, Sydney, NSW, AustraliaCentre for Research Excellence in Tuberculosis and the Marie Bashir Institute for Infectious Diseases and Biosecurity, The University of Sydney, Sydney, NSW, AustraliaThe Broad Institute of Harvard and MIT, Cambridge, MA, United StatesThe Broad Institute of Harvard and MIT, Cambridge, MA, United StatesCentre for Research Excellence in Tuberculosis and the Marie Bashir Institute for Infectious Diseases and Biosecurity, The University of Sydney, Sydney, NSW, AustraliaSydney School of Veterinary Science, The University of Sydney, Camden, NSW, AustraliaNSW Mycobacterium Reference Laboratory, Centre for Infectious Diseases and Microbiology Laboratory Services, Institute of Clinical Pathology and Medical Research – Pathology West, Sydney, NSW, AustraliaCentre for Research Excellence in Tuberculosis and the Marie Bashir Institute for Infectious Diseases and Biosecurity, The University of Sydney, Sydney, NSW, AustraliaThe Broad Institute of Harvard and MIT, Cambridge, MA, United StatesCentre for Research Excellence in Tuberculosis and the Marie Bashir Institute for Infectious Diseases and Biosecurity, The University of Sydney, Sydney, NSW, AustraliaMycobacteria have been classified into rapid and slow growing phenotypes, but the genetic factors that underlie these growth rate differences are not well understood. We compared the genomes of 157 mycobacterial species, representing all major branches of the mycobacterial phylogenetic tree to identify genes and operons enriched among rapid and slow growing mycobacteria. Overlaying growth phenotype on a phylogenetic tree based on 304 core genes suggested that ancestral mycobacteria had a rapid growth phenotype with a single major evolutionary separation into rapid and slow growing sub-genera. We identified 293 genes enriched among rapid growing sub-genera, including genes encoding for amino acid transport/metabolism (e.g., livFGMH operon) and transcription, as well as novel ABC transporters. Loss of the livFGMH and ABC transporter operons among slow growing species suggests that reduced cellular amino acid transport may be growth limiting. Comparative genomic analysis suggests that horizontal gene transfer, from non-mycobacterial genera, may have contributed to niche adaptation and pathogenicity, especially among slow growing species. Interestingly, the mammalian cell entry (mce) operon was found to be ubiquitous, irrespective of growth phenotype or pathogenicity, although protein sequence homology between rapid and slow growing species was low (<50%). This suggests that the mce operon was present in ancestral rapid growing species, but later adapted by slow growing species for use as a mechanism to establish an intra-cellular lifestyle.https://www.frontiersin.org/article/10.3389/fmicb.2019.03019/fullMycobacterium speciesgrowth phenotypeevolutioncomparative genomicsphylogenetic analysis |
| spellingShingle | Nathan L. Bachmann Nathan L. Bachmann Rauf Salamzade Abigail L. Manson Richard Whittington Richard Whittington Vitali Sintchenko Vitali Sintchenko Ashlee M. Earl Ben J. Marais Key Transitions in the Evolution of Rapid and Slow Growing Mycobacteria Identified by Comparative Genomics Frontiers in Microbiology Mycobacterium species growth phenotype evolution comparative genomics phylogenetic analysis |
| title | Key Transitions in the Evolution of Rapid and Slow Growing Mycobacteria Identified by Comparative Genomics |
| title_full | Key Transitions in the Evolution of Rapid and Slow Growing Mycobacteria Identified by Comparative Genomics |
| title_fullStr | Key Transitions in the Evolution of Rapid and Slow Growing Mycobacteria Identified by Comparative Genomics |
| title_full_unstemmed | Key Transitions in the Evolution of Rapid and Slow Growing Mycobacteria Identified by Comparative Genomics |
| title_short | Key Transitions in the Evolution of Rapid and Slow Growing Mycobacteria Identified by Comparative Genomics |
| title_sort | key transitions in the evolution of rapid and slow growing mycobacteria identified by comparative genomics |
| topic | Mycobacterium species growth phenotype evolution comparative genomics phylogenetic analysis |
| url | https://www.frontiersin.org/article/10.3389/fmicb.2019.03019/full |
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