- Micrococcus luteus. - 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.. - 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.. - 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.. - 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. - The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. - The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.. - luteus and highlighted that gene gain/loss events and extensive recombination events played key roles in the genome evolution. - Micrococcus luteus, the type species of the genus Micro- coccus (family Micrococcaceae, order Micrococcales), is a high GC Gram-positive coccus of the phylum Actinobac- teria [1]. - luteus revealed a circular chromosome with one of the smallest genomes of free- living actinobacteria and an abnormally high number of transposable elements [12]. - luteus and the genomic events that contribute to the ecological adaptation need further study.. - luteus and to un- cover the evolutionary events that may contribute to the genomic diversity. - luteus and the other species of Micrococcus.. - Each genome contained 159 to 315 identi- fiable insertion sequences (ISs), accounting for 7.22 to 13.4% of the genome (mean 8.51. - mean 8.3) that were 3.1 to 96.2 kbp in size, which together accounted for an average of 6.6% of the whole genome (ranging from 2.3 to 11.4. - 1 Pairwise genome-wide ANI values and maximum-likelihood phylogeny of the genus Micrococcus. - ANI values calculated by the pyani are color-coded according to the provided scale bar.. - b Maximum-likelihood phylogeny generated from concatenated 174 single-copy core genes with no evidence of recombination from PhiPack of the 76 Micrococcus strains, including three outgroup strains. - These core VFs might play important roles in the patho- genicity of M. - Copy number variation of the VF genes was also found. - The expansion of VF genes may promote the pathogenicity of the harbor- ing strains.. - Additionally, an aminoglycoside phos- photransferase encoded by strA, which confers aminoglycoside-resistance, was found in 59.1% (n = 39) of the strains. - To explore the entire genomic repertoire of the M.. - luteus population, estimates of the cloud (genes present in only one or two genomes), shell (genes present in 3–. - The core genome only represented 45.3 to 52.8% of the gene content of each strain, illustrating a relatively high degree of gen- omic diversity. - This core gene ratio was much lower than that of the actinobacterial species Streptomyces albidoflavus (65.3 to 73.0%, recalculated with the same clustering algorithm and parameters, intraspecies ANI >. - Furthermore, the cloud genes contained more than half of the pan-genome (4210 genes, 52.1%;. - Analysis of the pan-genome curve using a power-law regression model confirmed that the pan-genome was open (B pan = 0.5), as the curve did not approach a constant as more genomes were selected.. - We next performed a Clusters of Orthologous Groups (COG) functional classification for each orthologous group (OG) to define possible differences in the func- tions encoded by the soft-core, cloud and shell genomes of M. - 0.01, Fisher’s exact test), which may contribute to the intraspecies heterogeneity of the species, as these genes have been proved to play important roles in the acquisition of foreign DNA [34].. - To uncover the evolutionary process that led to the genomic diversity, we constructed a highly robust phylo- genomic maximum-likelihood (ML) tree of the 66 M.. - endophyticus strains (‘Micrococcus luteus’ AS2 and ‘Micrococcus luteus’. - Based on the phyloge- nomic tree, M. - 3 Phylogenetic tree and the population structure of the M. - This tree clearly showed three clades, which were the same as those in the core genome tree, indicating the existence of inter-clade gene content boundaries. - These results suggested that the separation between the three clades has emerged, both in the core and accessory genes.. - These three subpopulations corresponded to the three major clades on the phyloge- nomic tree. - It was noted that, the fourth ancestral subpopulation (POP4, yellow) existed in high proportions in all the three clades, with the highest proportion in the fourth subpop- ulation uncovered by the above Fastbaps analysis (i.e., strain NCTC 7563 in Clade II). - However, since POP4 accounted for only 47.5% of the genome of NCTC 7563, it is unclear whether POP4 can be represented by the branch of strain NCTC 7563. - luteus To unravel the evolutionary events that contributed to the intraspecies gene content differences, gene contents of all ancestral nodes on the phylogenomic tree were predicted and the numbers of gene gain and loss events that have occurred on all branches were calculated using a parsimony method (Figure S7). - Also, a relatively high number of gene content variances occurred at the divergence of the three major clades (77, 64 and 55 for Clades I to III, respectively), consistent. - Recombination, especially homologous recombination, is one of the main forces shaping bacterial evolution [37, 38]. - Here, a series of analyses were used to evaluate the extent of homologous recombination in the core genome of M. - the recombin- ation coverage (c), which indicates the proportion of sites in the genome whose diversity has come from re- combination events since its last common ancestor, was 0.46. - A summary of the parame- ters of M. - Among the 991 single-copy core genes, 628 genes (63.37%) showed significant evidence of genetic recom- bination, with P-values (computed from 1000 permuta- tions) lower than 0.05 in at least two of the three methods implemented in PhiPack [40]. - In order to investigate whether the genomic differences between clades are relevant to the habitat, the isolation resources of all strains were mapped to the phylogenomic tree (Fig. - c Distributions of the three recombination parameters for all pairs of genomes. - Names of some of the most frequently recombined genes are shown. - Micrococcus luteus This study. - HA strains were not clustered on the tree but rather widely distributed in all clades, indicating the inter-clade genetic difference was irrelevant to the habitat transition.. - A pan-genome-wide association study (pan- GWAS) revealed 101 accessory genes that were present in at least half of the strains from one habitat but no more than half from the other. - Sortases are enzymes responsible for covalent anchoring of specific proteins to the peptidoglycan of the cell wall of Gram-positive bacteria, performing critical biological functions that are required for the colonization and in- vasion of host tissues [51, 52]. - Sortases have also been considered as important virulence factors, as they play key roles in the infection process [53]. - However, the function of OG_1888 in the adaption to the NHA habitats is unknown. - 5 Distribution of the habitat-associated OGs. - absence of this OG is unrelated to the habitat. - The Abi system, ab- breviated for the phage abortive infection system, pro- vides a post-infection resistance mechanism that could block phage multiplication and result in the death of the infected bacterial cell upon phage infection [55–57]. - In addition, most of the previously re- ported cases due to M. - Consistently, our analyses showed that all of the total 66 genomes contained the rbpA gene, the product of which has been reported to confer basal levels of rifampicin resistance on Streptomy- ces coelicolor [61]. - 6 Genetic organizations of the regions containing habitat-associated genes. - due to the incomplete genome sequences for most strains, though only high-quality genome sequences (completeness >. - This high genome variability may contribute to the functional diversity of M. - luteus has di- verged into three well-differentiated clades, while popu- lation structure analysis revealed four admixed ancestral subpopulations, with three of them corresponding to the three clades, respectively, and the fourth (represented by strain NCTC 7563) corresponding to an unknown an- cestor. - In summary, while the population structure analysis supported the inter-clade differences, it suggested the existence of an unknown ancestor that contributed to the diversity of the species or the existence of the fourth, yet unsampled, clade. - Furthermore, consistent with the high proportion of admixture inferred from population assignment and also the numerous insertion sequences and transposases detected in the genomes, our study provides compelling evidence for high-level homologous recombination within M. - Recombination has been proved as an im- portant driver of the evolution of most prokaryotes, and acquisition of novel alleles of existing genes will also accelerate ecological adaptation of bacterial popu- lations [65, 66].. - Nevertheless, much of the inferred habitat- associated genes remain uncharted and/or await experi- mental verification. - In fact, we did not detect any clues to the existence of re- combination barriers between habitats, as there was no obvious difference in recombination parameters between datasets of HA, NHA, and all strains (Table 1). - However, the separation process seems to be suppressed probably because of the high-level recombin- ation and the strong diffusibility between niches.. - We performed comprehensive comparative genomic analyses of 66 Micrococcus luteus genomes. - Our study revealed high intraspecies genome diversity and exten- sive gene gain/loss events that contributed to the gen- ome diversity, and showed that extensive recombination played key roles in the evolution of the species. - This recent ecological differentiation appeared to be a process that was not re- lated to the early phylogenetic separation of different clades of the species. - To avoid the stat- istical deviation caused by highly similar strains or even multiple sequencing of the same strain (e.g., strain NCTC 2665), we considered genome pair redundant when ANI was higher than 99.9%. - luteus genomes were identified through BLASTp searches of the Comprehensive Anti- biotic Resistance Database (CARD) [81] and the VFDB [28], respectively, with E-values ≤1e-05 and Ha-value >. - In addition, PhiPack [40] was also used, by which potential recombination events were identified by having P-values lower than 0.05 in at least two of the three methods (PHI, Neighbor Similarity Score and Maximum Chi-Square) computed from 1000 permutations. - Identification of the habitat-associated genes. - Heatmap of the distributions of the putative VF genes in M. - Comparison of the soft-core, shell and cloud genomes of M. - YSL and BBX contributed to conception and design of the study. - The first case of native mitral valve endocarditis due to Micrococcus luteus and review of the literature. - Native valve infective endocarditis due to Micrococcus luteus in a non-Hodgkin's lymphoma patient. - Micrococcus luteus as a cause of recurrent bacteremia. - The rpf gene of Micrococcus luteus encodes an essential secreted growth factor. - Genome sequence of the Fleming strain of Micrococcus luteus, a simple free-living actinobacterium. - Comparative genomics analysis of Streptomyces species reveals their adaptation to the marine. - Urease is an essential component of the acid response network of Staphylococcus aureus and is required for a persistent murine kidney infection. - The outer membrane localization of the Neisseria gonorrhoeae MsrA/B is involved in survival against reactive oxygen species. - Characterization of the methionine sulfoxide reductase activities of PILB, a probable virulence factor from Neisseria meningitidis. - Recombination and the nature of bacterial speciation. - DNA sequence and analysis of the bet genes encoding the osmoregulatory choline-glycine betaine pathway of Escherichia coli. - Evolution of the natural transformation protein, ComEC, in bacteria. - AbiEi binds cooperatively to the type IV abiE toxin-antitoxin operator via a positively-charged surface and causes DNA bending and negative autoregulation. - The role of glyoxalase I in the detoxification of methylglyoxal and in the activation of the KefB K + efflux system in Escherichia coli. - Native valve endocarditis due to Micrococcus luteus: a case report and review of the literature. - Studies on the genomic heterogeneity of Micrococcus luteus strains by macro-restriction analysis using pulsed-field gel electrophoresis. - Population genomics of early events in the ecological differentiation of bacteria
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