Comparative genomics reveals broad genetic diversity, extensive recombination and nascent ecological adaptation in Micrococcus luteus
Abstract Background Micrococcus luteus is a group of actinobacteria that is widely used in biotechnology and is being thought as an emerging nosocomial pathogen. With one of the smallest genomes of free-living actinobacteria, it is found in a wide range of environments, but intraspecies genetic dive...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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BMC
2021-02-01
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| Series: | BMC Genomics |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12864-021-07432-5 |
| _version_ | 1819050516378812416 |
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| author | Yisong Li Zhong-Zhi Sun Jin-Cheng Rong Bin-Bin Xie |
| author_facet | Yisong Li Zhong-Zhi Sun Jin-Cheng Rong Bin-Bin Xie |
| author_sort | Yisong Li |
| collection | DOAJ |
| description | Abstract Background Micrococcus luteus is a group of actinobacteria that is widely used in biotechnology and is being thought as an emerging nosocomial pathogen. With one of the smallest genomes of free-living actinobacteria, it is found in a wide range of environments, but intraspecies genetic diversity and adaptation strategies to various environments remain unclear. Here, comparative genomics, phylogenomics, and genome-wide association studies were used to investigate the genomic diversity, evolutionary history, and the potential ecological differentiation of the species. Results High-quality genomes of 66 M. luteus strains were downloaded from the NCBI GenBank database and core and pan-genome analysis revealed a considerable intraspecies heterogeneity. Phylogenomic analysis, gene content comparison, and average nucleotide identity calculation consistently indicated that the species has diverged into three well-differentiated clades. Population structure analysis further suggested the existence of an unknown ancestor or the fourth, yet unsampled, clade. Reconstruction of gene gain/loss events along the evolutionary history revealed both early events that contributed to the inter-clade divergence and recent events leading to the intra-clade diversity. We also found convincing evidence that recombination has played a key role in the evolutionary process of the species, with upto two-thirds of the core genes having been affected by recombination. Furthermore, distribution of mammal-associated strains (including pathogens) on the phylogenetic tree suggested that the last common ancestor had a free-living lifestyle, and a few recently diverged lineages have developed a mammal-associated lifestyle separately. Consistently, genome-wide association analysis revealed that mammal-associated strains from different lineages shared genes functionally relevant to the host-associated lifestyle, indicating a recent ecological adaption to the new host-associated habitats. Conclusions These results revealed high intraspecies genomic diversity of M. luteus and highlighted that gene gain/loss events and extensive recombination events played key roles in the genome evolution. Our study also indicated that, as a free-living species, some lineages have recently developed or are developing a mammal-associated lifestyle. This study provides insights into the mechanisms that drive the genome evolution and adaption to various environments of a bacterial species. |
| first_indexed | 2024-12-21T11:49:17Z |
| format | Article |
| id | doaj.art-deee8baa6a1b46f8b8ce6e7ca792a19f |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-12-21T11:49:17Z |
| publishDate | 2021-02-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Genomics |
| spelling | doaj.art-deee8baa6a1b46f8b8ce6e7ca792a19f2022-12-21T19:05:06ZengBMCBMC Genomics1471-21642021-02-0122111410.1186/s12864-021-07432-5Comparative genomics reveals broad genetic diversity, extensive recombination and nascent ecological adaptation in Micrococcus luteusYisong Li0Zhong-Zhi Sun1Jin-Cheng Rong2Bin-Bin Xie3Microbial Technology Institute and State Key Laboratory of Microbial Technology, Shandong UniversityMicrobial Technology Institute and State Key Laboratory of Microbial Technology, Shandong UniversityMicrobial Technology Institute and State Key Laboratory of Microbial Technology, Shandong UniversityMicrobial Technology Institute and State Key Laboratory of Microbial Technology, Shandong UniversityAbstract Background Micrococcus luteus is a group of actinobacteria that is widely used in biotechnology and is being thought as an emerging nosocomial pathogen. With one of the smallest genomes of free-living actinobacteria, it is found in a wide range of environments, but intraspecies genetic diversity and adaptation strategies to various environments remain unclear. Here, comparative genomics, phylogenomics, and genome-wide association studies were used to investigate the genomic diversity, evolutionary history, and the potential ecological differentiation of the species. Results High-quality genomes of 66 M. luteus strains were downloaded from the NCBI GenBank database and core and pan-genome analysis revealed a considerable intraspecies heterogeneity. Phylogenomic analysis, gene content comparison, and average nucleotide identity calculation consistently indicated that the species has diverged into three well-differentiated clades. Population structure analysis further suggested the existence of an unknown ancestor or the fourth, yet unsampled, clade. Reconstruction of gene gain/loss events along the evolutionary history revealed both early events that contributed to the inter-clade divergence and recent events leading to the intra-clade diversity. We also found convincing evidence that recombination has played a key role in the evolutionary process of the species, with upto two-thirds of the core genes having been affected by recombination. Furthermore, distribution of mammal-associated strains (including pathogens) on the phylogenetic tree suggested that the last common ancestor had a free-living lifestyle, and a few recently diverged lineages have developed a mammal-associated lifestyle separately. Consistently, genome-wide association analysis revealed that mammal-associated strains from different lineages shared genes functionally relevant to the host-associated lifestyle, indicating a recent ecological adaption to the new host-associated habitats. Conclusions These results revealed high intraspecies genomic diversity of M. luteus and highlighted that gene gain/loss events and extensive recombination events played key roles in the genome evolution. Our study also indicated that, as a free-living species, some lineages have recently developed or are developing a mammal-associated lifestyle. This study provides insights into the mechanisms that drive the genome evolution and adaption to various environments of a bacterial species.https://doi.org/10.1186/s12864-021-07432-5Micrococcus luteusPopulation genomicsPan-genomeIntraspecies diversityRecombinationAdaptive evolution |
| spellingShingle | Yisong Li Zhong-Zhi Sun Jin-Cheng Rong Bin-Bin Xie Comparative genomics reveals broad genetic diversity, extensive recombination and nascent ecological adaptation in Micrococcus luteus BMC Genomics Micrococcus luteus Population genomics Pan-genome Intraspecies diversity Recombination Adaptive evolution |
| title | Comparative genomics reveals broad genetic diversity, extensive recombination and nascent ecological adaptation in Micrococcus luteus |
| title_full | Comparative genomics reveals broad genetic diversity, extensive recombination and nascent ecological adaptation in Micrococcus luteus |
| title_fullStr | Comparative genomics reveals broad genetic diversity, extensive recombination and nascent ecological adaptation in Micrococcus luteus |
| title_full_unstemmed | Comparative genomics reveals broad genetic diversity, extensive recombination and nascent ecological adaptation in Micrococcus luteus |
| title_short | Comparative genomics reveals broad genetic diversity, extensive recombination and nascent ecological adaptation in Micrococcus luteus |
| title_sort | comparative genomics reveals broad genetic diversity extensive recombination and nascent ecological adaptation in micrococcus luteus |
| topic | Micrococcus luteus Population genomics Pan-genome Intraspecies diversity Recombination Adaptive evolution |
| url | https://doi.org/10.1186/s12864-021-07432-5 |
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