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Volume 10, Issue 8

Comparative genomic analysis identifies potential adaptive variation in Open Access

Abstract

is associated with respiratory disease in wild and domestic Caprinae globally, with wide variation in disease outcomes within and between host species. To gain insight into phylogenetic structure and mechanisms of pathogenicity for this bacterial species, we compared genomes for 99 samples from 6 countries (Australia, Bosnia and Herzegovina, Brazil, China, France and USA) and 4 host species (domestic sheep, domestic goats, bighorn sheep and caribou). Core genome sequences of assemblies from domestic sheep and goats fell into two well-supported phylogenetic clades that are divergent enough to be considered different bacterial species, consistent with each of these two clades having an evolutionary origin in separate host species. Genome assemblies from bighorn sheep and caribou also fell within these two clades, indicating multiple spillover events, most commonly from domestic sheep. Pangenome analysis indicated a high percentage (91.4 %) of accessory genes (i.e. genes found only in a subset of assemblies) compared to core genes (i.e. genes found in all assemblies), potentially indicating a propensity for this pathogen to adapt to within-host conditions. In addition, many genes related to carbon metabolism, which is a virulence factor for Mycoplasmas, showed evidence for homologous recombination, a potential signature of adaptation. The presence or absence of annotated genes was very similar between sheep and goat clades, with only two annotated genes significantly clade-associated. However, three genome assemblies from asymptomatic caribou in Alaska formed a highly divergent subclade within the sheep clade that lacked 23 annotated genes compared to other assemblies, and many of these genes had functions related to carbon metabolism. Overall, our results suggest that adaptation of has involved evolution of carbon metabolism pathways and virulence mechanisms related to those pathways. The genes involved in these pathways, along with other genes identified as potentially involved in virulence in this study, are potential targets for future investigation into a possible genomic basis for the high variation observed in disease outcomes within and between wild and domestic host species.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Capra hircus , dN/dS , homologous recombination , Ovis aries , Ovis canadensis and pangenome
Funding
This study was supported by the:
  • Idaho Department of Fish and Game
    • Principal Award Recipient: KimberlyR. Andrews
© 2024 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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References

  1. Balish M, Bertaccini A, Blanchard A, Brown D, Browning G et al. Recommended rejection of the names malacoplasma gen. nov., mesomycoplasma gen. nov., metamycoplasma gen. nov., metamycoplasmataceae fam. nov., mycoplasmoidaceae fam. nov., mycoplasmoidales ord. nov., mycoplasmoides gen. nov., mycoplasmopsis gen. nov. [gupta, sawnani, adeolu, alnajar and oren 2018] and all proposed species comb. nov. placed therein. Int J Syst Evol Microbiol 2019; 69:3650–3653 [View Article]
     [Google Scholar]
  2. Gupta RS, Son J, Oren A. A phylogenomic and molecular markers based taxonomic framework for members of the order Entomoplasmatales: proposal for an emended order Mycoplasmatales containing the family Spiroplasmataceae and emended family Mycoplasmataceae comprised of six genera. Antonie van Leeuwenhoek 2019; 112:561–588 [View Article] [PubMed]
     [Google Scholar]
  3. Jaÿ M, Ambroset C, Tricot A, Colin A, Tardy F. Population structure and antimicrobial susceptibility of Mycoplasma ovipneumoniae isolates in France. Vet Microbiol 2020; 248:108828 [View Article] [PubMed]
     [Google Scholar]
  4. Nicholas RAJ, Ayling RD, Loria GR. Ovine mycoplasmal infections. Small Ruminant Res 2008; 76:92–98 [View Article]
     [Google Scholar]
  5. Maksimović Z, Rifatbegović M, Loria GR, Nicholas RAJ. Mycoplasma ovipneumoniae: a most variable pathogen. Pathogens 2022; 11:1477 [View Article] [PubMed]
     [Google Scholar]
  6. Manlove K, Branan M, Baker K, Bradway D, Cassirer EF et al. Risk factors and productivity losses associated with Mycoplasma ovipneumoniae infection in United States domestic sheep operations. Prev Vet Med 2019; 168:30–38 [View Article] [PubMed]
     [Google Scholar]
  7. Besser TE, Levy J, Ackerman M, Nelson D, Manlove K et al. A pilot study of the effects of Mycoplasma ovipneumoniae exposure on domestic lamb growth and performance. PLoS One 2019; 14:e0207420 [View Article] [PubMed]
     [Google Scholar]
  8. DaMassa AJ, Wakenell PS, Brooks DL. Mycoplasmas of goats and sheep. J Vet Diagn Invest 1992; 4:101–113 [View Article] [PubMed]
     [Google Scholar]
  9. Alley MR, Ionas G, Clarke JK. Chronic non-progressive pneumonia of sheep in New Zealand - a review of the role of Mycoplasma ovipneumoniae. N Z Vet J 1999; 47:155–160 [View Article] [PubMed]
     [Google Scholar]
  10. Besser TE, Cassirer EF, Yamada C, Potter KA, Herndon C et al. Survival of bighorn sheep (Ovis canadensis) commingled with domestic sheep (Ovis aries) in the absence of Mycoplasma ovipneumoniae. J Wildl Dis 2012; 48:168–172 [View Article] [PubMed]
     [Google Scholar]
  11. Kamath PL, Manlove K, Cassirer EF, Cross PC, Besser TE. Genetic structure of Mycoplasma ovipneumoniae informs pathogen spillover dynamics between domestic and wild Caprinae in the western United States. Sci Rep 2019; 9:15318 [View Article] [PubMed]
     [Google Scholar]
  12. Handeland K, Tengs T, Kokotovic B, Vikøren T, Ayling RD et al. Mycoplasma ovipneumoniae - a primary cause of severe pneumonia epizootics in the Norwegian Muskox (Ovibos moschatus) population. PLoS One 2014; 9:e106116 [View Article] [PubMed]
     [Google Scholar]
  13. Besser TE, Highland M, Baker K, Cassirer EF, Anderson NJ et al. Causes of pneumonia epizootics among bighorn sheep, Western United States, 2008–2010. Emerg Infect Dis 2012; 18:406–414 [View Article]
     [Google Scholar]
  14. Black SR, Barker IK, Mehren KG, Crawshaw GJ, Rosendal S et al. An epizootic of Mycoplasma ovipneumoniae infection in captive Dall’s sheep (Ovis dalli dalli). J Wildl Dis 1988; 24:627–635 [View Article] [PubMed]
     [Google Scholar]
  15. Cassirer EF, Manlove KR, Almberg ES, Kamath PL, Cox M et al. Pneumonia in bighorn sheep: risk and resilience. J Wildl Manag 2018; 82:32–45 [View Article]
     [Google Scholar]
  16. Manlove K, Cassirer EF, Cross PC, Plowright RK, Hudson PJ. Disease introduction is associated with a phase transition in bighorn sheep demographics. Ecology 2016; 97:2593–2602 [View Article] [PubMed]
     [Google Scholar]
  17. Plowright RK, Manlove KR, Besser TE, Páez DJ, Andrews KR et al. Age-specific infectious period shapes dynamics of pneumonia in bighorn sheep. Ecol Lett 2017; 20:1325–1336 [View Article] [PubMed]
     [Google Scholar]
  18. Garwood TJ, Lehman CP, Walsh DP, Cassirer EF, Besser TE et al. Removal of chronic Mycoplasma ovipneumoniae carrier ewes eliminates pneumonia in a bighorn sheep population. Ecol Evol 2020; 10:3491–3502 [View Article] [PubMed]
     [Google Scholar]
  19. Johnson BM, Stroud-Settles J, Roug A, Manlove K. Disease ecology of a low-virulence Mycoplasma ovipneumoniae strain in a free-ranging desert bighorn sheep population. Animals 2022; 12:1029 [View Article]
     [Google Scholar]
  20. Walsh DP, Felts BL, Cassirer EF, Besser TE, Jenks JA. Host vs. pathogen evolutionary arms race: effects of exposure history on individual response to a genetically diverse pathogen. Front Ecol Evol 2023; 10: [View Article]
     [Google Scholar]
  21. Besser TE, Cassirer EF, Lisk A, Nelson D, Manlove KR et al. Natural history of a bighorn sheep pneumonia epizootic: source of infection, course of disease, and pathogen clearance. Ecol Evol 2021; 11:14366–14382 [View Article] [PubMed]
     [Google Scholar]
  22. Niang M, Rosenbusch RF, DeBey MC, Niyo Y, Andrews JJ et al. Field isolates of Mycoplasma ovipneumoniae exhibit distinct cytopathic effects in ovine tracheal organ cultures. J Vet Med Ser A 1998; 45:29–40 [View Article] [PubMed]
     [Google Scholar]
  23. Yang FL, Tang C, Wang Y, Zhang HR, Yue H. Genome sequence of Mycoplasma ovipneumoniae strain SC01. J Bacteriol 2011; 193:5018 [View Article]
     [Google Scholar]
  24. Einarsdottir T, Gunnarsson E, Hjartardottir S. Icelandic ovine Mycoplasma ovipneumoniae are variable bacteria that induce limited immune responses in vitro and in vivo. J Med Microbiol 2018; 67:1480–1490 [View Article] [PubMed]
     [Google Scholar]
  25. Dudek K, Sevimli U, Migliore S, Jafarizadeh A, Loria GR et al. Vaccines for Mycoplasma diseases of small ruminants: a neglected area of research. Pathogens 2022; 11:75 [View Article] [PubMed]
     [Google Scholar]
  26. Jiang Z, Song F, Li Y, Xue D, Zhao N et al. Capsular polysaccharide of Mycoplasma ovipneumoniae induces sheep airway epithelial cell apoptosis via ROS-dependent JNK/P38 MAPK pathways.. Oxid Med Cell Longev 2017; 2017:6175841 [View Article] [PubMed]
     [Google Scholar]
  27. Jiang ZJ, Song FY, Li YN, Xue D, Deng GC et al. Capsular polysaccharide is a main component of Mycoplasma ovipneumoniae in the pathogen-induced toll-like receptor-mediated inflammatory responses in sheep airway epithelial cells. Mediators Inflamm 2017; 2017:1–15 [View Article]
     [Google Scholar]
  28. Li Y, Wang R, Sun W, Song Z, Bai F et al. Comparative genomics analysis of Mycoplasma capricolum subsp. capripneumoniae 87001. Genomics 2020; 112:615–620 [View Article]
     [Google Scholar]
  29. Chen S, Hao H, Zhao P, Liu Y, Chu Y. Genome-wide analysis of Mycoplasma bovirhinis GS01 reveals potential virulence factors and phylogenetic relationships. G3 2018; 8:1417–1424 [View Article]
     [Google Scholar]
  30. Trueeb BS, Gerber S, Maes D, Gharib WH, Kuhnert P. Tn-sequencing of Mycoplasma hyopneumoniae and Mycoplasma hyorhinis mutant libraries reveals non-essential genes of porcine mycoplasmas differing in pathogenicity. Vet Res 2019; 50:55 [View Article] [PubMed]
     [Google Scholar]
  31. Brown DR, Farmerie WG, May M, Benders GA, Durkin AS et al. Genome sequences of Mycoplasma alligatoris A21JP2T and Mycoplasma crocodyli MP145T. J Bacteriol 2011; 193:2892–2893 [View Article] [PubMed]
     [Google Scholar]
  32. Liu W, Xiao S, Li M, Guo S, Li S et al. Comparative genomic analyses of Mycoplasma hyopneumoniae pathogenic 168 strain and its high-passaged attenuated strain. BMC Genomics 2013; 14:80 [View Article] [PubMed]
     [Google Scholar]
  33. Szczepanek SM, Tulman ER, Gorton TS, Liao X, Lu Z et al. Comparative genomic analyses of attenuated strains of Mycoplasma gallisepticum. Infect Immun 2010; 78:1760–1771 [View Article] [PubMed]
     [Google Scholar]
  34. Sheppard SK, Guttman DS, Fitzgerald JR. Population genomics of bacterial host adaptation. Nat Rev Genet 2018; 19:549–565 [View Article] [PubMed]
     [Google Scholar]
  35. Keen EC, Choi J, Wallace MA, Azar M, Mejia-Chew CR et al. Comparative genomics of Mycobacterium avium complex reveals signatures of environment-specific adaptation and community acquisition. mSystems 2021; 6:e0119421 [View Article] [PubMed]
     [Google Scholar]
  36. Wang J, Li Y, Pinto-Tomás AA, Cheng K, Huang Y. Habitat adaptation drives speciation of a Streptomyces species with distinct habitats and disparate geographic origins. mBio 2022; 13:e0278121 [View Article] [PubMed]
     [Google Scholar]
  37. Maksimović Z, De la Fe C, Amores J, Gómez-Martín Á, Rifatbegović M. Comparison of phenotypic and genotypic profiles among caprine and ovine Mycoplasma ovipneumoniae strains. Vet Rec 2017; 180:180 [View Article] [PubMed]
     [Google Scholar]
  38. Parham K, Churchward CP, McAuliffe L, Nicholas RAJ, Ayling RD. A high level of strain variation within the Mycoplasma ovipneumoniae population of the UK has implications for disease diagnosis and management. Vet Microbiol 2006; 118:83–90 [View Article] [PubMed]
     [Google Scholar]
  39. Cassirer EF, Manlove KR, Plowright RK, Besser TE. Evidence for strain‐specific immunity to pneumonia in bighorn sheep. J Wildl Manag 2017; 81:133–143 [View Article]
     [Google Scholar]
  40. Besser TE, Cassirer EF, Potter KA, Foreyt WJ. Exposure of bighorn sheep to domestic goats colonized with Mycoplasma ovipneumoniae induces sub-lethal pneumonia. PLoS One 2017; 12:e0178707 [View Article] [PubMed]
     [Google Scholar]
  41. Foreyt WJ, Jenkins EJ, Appleyard GD. Transmission of lungworms (Muellerius capillaris) from domestic goats to bighorn sheep on common pasture. J Wildl Dis 2009; 45:272–278 [View Article] [PubMed]
     [Google Scholar]
  42. Wehausen JD. Domestic sheep, bighorn sheep, and respiratory disease: a review of the experimental evidence. California Fish Game 2011; 97:7–24
     [Google Scholar]
  43. Lieske CL, Gerlach R, Francis M, Beckmen KB. Multilocus sequence typing of Mycoplasma ovipneumoniae detected in Dall’s sheep (Ovis dalli dalli) and Caribou (Rangifer tarandus grantii) in Alaska, USA. J Wildl Dis 2022; 58:625–630 [View Article] [PubMed]
     [Google Scholar]
  44. May M, Brown DR. Diversifying and stabilizing selection of sialidase and N-acetylneuraminate catabolism in Mycoplasma synoviae. . J Bacteriol 2009; 191:3588–3593 [View Article] [PubMed]
     [Google Scholar]
  45. Cao P, Guo D, Liu J, Jiang Q, Xu Z et al. Genome-wide analyses reveal genes subject to positive selection in Pasteurella multocida. Front Microbiol 2017; 8: [View Article]
     [Google Scholar]
  46. González-Torres P, Rodríguez-Mateos F, Antón J, Gabaldón T. Impact of homologous recombination on the evolution of prokaryotic core genomes. mBio 2019; 10:e02494-18 [View Article] [PubMed]
     [Google Scholar]
  47. Arnold BJ, Huang IT, Hanage WP. Horizontal gene transfer and adaptive evolution in bacteria. Nat Rev Microbiol 2022; 20:206–218 [View Article] [PubMed]
     [Google Scholar]
  48. Cottew GS. Caprine-ovine mycoplasmas. In The Mycoplasmas, Vol II, Human and Animal Mycoplasmas New York: Academic Press, Inc; 1979 pp 103–132 [View Article]
     [Google Scholar]
  49. Carmichael LE, St George TD, Sullivan ND, Horsfall N. Isolation, propagation, and characterization studies of an ovine Mycoplasma responsible for proliferative interstitial pneumonia. Cornell Vet 1972; 62:654–679 [PubMed]
     [Google Scholar]
  50. Jennings-Gaines JE, Edwards WH, Wood ME, Fox KA, Wolfe LL et al. An improved method for culturing Mycoplasma ovipneumoniae from field samples. Biennial Symposium of the Northern Wild Sheep and Goat Council 2016; 20:83–88
     [Google Scholar]
  51. Kim D, Song L, Breitwieser FP, Salzberg SL. Centrifuge: rapid and sensitive classification of metagenomic sequences. Genom Res 2016; 26:1721–1729 [View Article] [PubMed]
     [Google Scholar]
  52. Wick RR, Judd LM, Cerdeira LT, Hawkey J, Méric G et al. Trycycler: consensus long-read assemblies for bacterial genomes. Genome Biol 2021; 22:266 [View Article] [PubMed]
     [Google Scholar]
  53. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 2014; 9:e112963 [View Article] [PubMed]
     [Google Scholar]
  54. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article] [PubMed]
     [Google Scholar]
  55. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 2015; 25:1043–1055 [View Article] [PubMed]
     [Google Scholar]
  56. Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun 2018; 9:5114 [View Article] [PubMed]
     [Google Scholar]
  57. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
     [Google Scholar]
  58. Hyatt D, Chen G-L, Locascio PF, Land ML, Larimer FW et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinform 2010; 11:119 [View Article] [PubMed]
     [Google Scholar]
  59. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J et al. BLAST+: architecture and applications. BMC Bioinform 2009; 10:421 [View Article] [PubMed]
     [Google Scholar]
  60. Finn RD, Clements J, Eddy SR. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 2011; 39:W29–W37 [View Article] [PubMed]
     [Google Scholar]
  61. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015; 31:3691–3693 [View Article] [PubMed]
     [Google Scholar]
  62. Löytynoja A. Phylogeny-aware alignment with PRANK. In Russell D. eds Multiple Sequence Alignment Methods Methods in Molecular Biology (Methods and Protocols Totowa, NJ: Humana Press; 2014 pp 155–170 [View Article]
     [Google Scholar]
  63. Cantalapiedra CP, Hernández-Plaza A, Letunic I, Bork P, Huerta-Cepas J. eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol Biol Evol 2021; 38:5825–5829 [View Article] [PubMed]
     [Google Scholar]
  64. Huerta-Cepas J, Szklarczyk D, Heller D, Hernández-Plaza A, Forslund SK et al. eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res 2019; 47:D309–D314 [View Article] [PubMed]
     [Google Scholar]
  65. Ruiz-Perez CA, Conrad RE, Konstantinidis KT. MicrobeAnnotator: a user-friendly, comprehensive functional annotation pipeline for microbial genomes. BMC Bioinform 2021; 22:11 [View Article] [PubMed]
     [Google Scholar]
  66. Gaeta NC, de Sá Guimarães AM, Timenetsky J, Clouser S, Gregory L et al. The first Mycoplasma ovipneumoniae recovered from a sheep with respiratory disease in Brazil - draft genome and genomic analysis. Vet Res Commun 2022; 46:1311–1318 [View Article] [PubMed]
     [Google Scholar]
  67. Buchfink B, Reuter K, Drost H-G. Sensitive protein alignments at tree-of-life scale using DIAMOND. Nat Methods 2021; 18:366–368 [View Article] [PubMed]
     [Google Scholar]
  68. Liu B, Zheng D, Jin Q, Chen L, Yang J. VFDB 2019: a comparative pathogenomic platform with an interactive web interface. Nucleic Acids Res 2018; 47:D687–D692 [View Article] [PubMed]
     [Google Scholar]
  69. Chen L, Yang J, Yu J, Yao Z, Sun L et al. VFDB: a reference database for bacterial virulence factors. Nucleic Acids Res 2005; 33:D325–D328 [View Article] [PubMed]
     [Google Scholar]
  70. Yiwen C, Yueyue W, Lianmei Q, Cuiming Z, Xiaoxing Y. Infection strategies of mycoplasmas: unraveling the panoply of virulence factors. Virulence 2021; 12:788–817 [View Article] [PubMed]
     [Google Scholar]
  71. Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A. RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 2019; 35:4453–4455 [View Article] [PubMed]
     [Google Scholar]
  72. Perron GG, Lee AEG, Wang Y, Huang WE, Barraclough TG. Bacterial recombination promotes the evolution of multi-drug-resistance in functionally diverse populations. Proc R Soc B 2012; 279:1477–1484 [View Article]
     [Google Scholar]
  73. Cavassim MIA, Andersen SU, Bataillon T, Schierup MH. Recombination facilitates adaptive evolution in rhizobial soil bacteria. Mol Biol Evol 2021; 38:5480–5490 [View Article] [PubMed]
     [Google Scholar]
  74. Hsieh Y-C, Li S-W, Chen Y-Y, Kuo C-C, Chen Y-C et al. Global genome diversity and recombination in Mycoplasma pneumoniae. Emerg Infect Dis 2022; 28:111–117 [View Article] [PubMed]
     [Google Scholar]
  75. Mostowy R, Croucher NJ, Andam CP, Corander J, Hanage WP et al. Efficient inference of recent and ancestral recombination within bacterial populations. Mol Biol Evol 2017; 34:1167–1182 [View Article] [PubMed]
     [Google Scholar]
  76. Corander J, Waldmann P, Sillanpää MJ. Bayesian analysis of genetic differentiation between populations. Genetics 2003; 163:367–374 [View Article] [PubMed]
     [Google Scholar]
  77. Yang ZH. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 2007; 24:1586–1591 [View Article]
     [Google Scholar]
  78. Melton AE, Chen S, Zhao Y, Fu C, Xiang Q-YJ et al. Genetic insights into the evolution of genera with the eastern Asia-eastern North America floristic disjunction: a transcriptomics analysis. Am J Bot 2020; 107:1736–1748 [View Article] [PubMed]
     [Google Scholar]
  79. Martinez-Gutierrez CA, Aylward FO. Strong purifying selection is associated with genome streamlining in epipelagic Marinimicrobia. Genome Biol Evol 2019; 11:2887–2894 [View Article] [PubMed]
     [Google Scholar]
  80. Brynildsrud O, Bohlin J, Scheffer L, Eldholm V. Rapid scoring of genes in microbial pan-genome-wide association studies with Scoary. Genome Biol 2016; 17:238 [View Article] [PubMed]
     [Google Scholar]
  81. San JE, Baichoo S, Kanzi A, Moosa Y, Lessells R et al. Current affairs of microbial genome-wide association studies: approaches, bottlenecks and analytical pitfalls. Front Microbiol 2019; 10:3119 [View Article] [PubMed]
     [Google Scholar]
  82. Couvin D, Bernheim A, Toffano-Nioche C, Touchon M, Michalik J et al. CRISPRCasFinder, an update of CRISRFinder, includes a portable version, enhanced performance and integrates search for Cas proteins. Nucleic Acids Res 2018; 46:W246–W251 [View Article] [PubMed]
     [Google Scholar]
  83. Abby SS, Néron B, Ménager H, Touchon M, Rocha EPC. MacSyFinder: a program to mine genomes for molecular systems with an application to CRISPR-Cas systems. PLoS One 2014; 9:e110726 [View Article] [PubMed]
     [Google Scholar]
  84. Grissa I, Vergnaud G, Pourcel C. CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 2007; 35:W52–W57 [View Article] [PubMed]
     [Google Scholar]
  85. Mizuki H, Shimoyama Y, Ishikawa T, Sasaki M. A genomic sequence of the type II-A clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR-associated system in Mycoplasma salivarium strain ATCC 29803. J Oral Microbiol 2022; 14:2008153 [View Article] [PubMed]
     [Google Scholar]
  86. Alexa A, Rahnenführer J. TopGO: enrichment analysis for gene ontology. R package version 2.50.0; 2022
  87. UniProt C UniProt: the universal protein knowledgebase in 2023. Nucleic Acids Res 2023; 51:D523–D531
     [Google Scholar]
  88. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article] [PubMed]
     [Google Scholar]
  89. Paradis E, Schliep K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 2019; 35:526–528 [View Article] [PubMed]
     [Google Scholar]
  90. Preska Steinberg A, Lin M, Kussell E. Core genes can have higher recombination rates than accessory genes within global microbial populations. eLife 2022; 11:e78533 [View Article] [PubMed]
     [Google Scholar]
  91. McInerney JO, McNally A, O’Connell MJ. Why prokaryotes have pangenomes. Nat Microbiol 2017; 2:17040 [View Article] [PubMed]
     [Google Scholar]
  92. Schmidl SR, Otto A, Lluch-Senar M, Piñol J, Busse J et al. A trigger enzyme in Mycoplasma pneumoniae: impact of the glycerophosphodiesterase GlpQ on virulence and gene expression. PLoS Pathog 2011; 7:e1002263 [View Article]
     [Google Scholar]
  93. Blötz C, Stülke J. Glycerol metabolism and its implication in virulence in Mycoplasma. . FEMS Microbiol Rev 2017; 41:640–652 [View Article] [PubMed]
     [Google Scholar]
  94. Gupta R, Chatterjee D, Glickman MS, Shuman S. Division of labor among Mycobacterium smegmatis RNase H enzymes: RNase H1 activity of RnhA or RnhC is essential for growth whereas RnhB and RnhA guard against killing by hydrogen peroxide in stationary phase. Nucleic Acids Res 2016; 45:1–14 [View Article] [PubMed]
     [Google Scholar]
  95. Zhu L, Shahid MA, Markham J, Browning GF, Noormohammadi AH et al. Comparative genomic analyses of Mycoplasma synoviae vaccine strain MS-H and its wild-type parent strain 86079/7NS: implications for the identification of virulence factors and applications in diagnosis of M. synoviae. Avian Pathol 2019; 48:537–548 [View Article] [PubMed]
     [Google Scholar]
  96. Akhtar AA, Turner DPJ. The role of bacterial ATP-binding cassette (ABC) transporters in pathogenesis and virulence: therapeutic and vaccine potential. Microb Pathog 2022; 171:105734 [View Article] [PubMed]
     [Google Scholar]
  97. Sun Y, Luo HW. Homologous recombination in core genomes facilitates marine bacterial adaptation. Appl Environ Microbiol 2018; 84: [View Article]
     [Google Scholar]
  98. Yahara K, Didelot X, Jolley KA, Kobayashi I, Maiden MCJ et al. The landscape of realized homologous recombination in pathogenic bacteria. Mol Biol Evol 2016; 33:456–471 [View Article]
     [Google Scholar]
  99. Michaels DL, Moneypenny CG, Shama SM, Leibowitz JA, May MA et al. Sialidase and N-acetylneuraminate catabolism in nutrition of Mycoplasma alligatoris. Microbiology 2019; 165:662–667 [View Article] [PubMed]
     [Google Scholar]
  100. Almagro-Moreno S, Boyd EF. Insights into the evolution of sialic acid catabolism among bacteria. BMC Evol Biol 2009; 9:118 [View Article] [PubMed]
     [Google Scholar]
  101. Ansari S, Kumar V, Bhatt DN, Irfan M, Datta A. N-acetylglucosamine sensing and metabolic engineering for attenuating human and plant pathogens. Bioengineering 2022; 9:64 [View Article] [PubMed]
     [Google Scholar]
  102. Bekő K, Kovács ÁB, Kreizinger Z, Marton S, Bányai K et al. Development of mismatch amplification mutation assay for the rapid differentiation of Mycoplasma gallisepticum K vaccine strain from field isolates. Avian Pathol 2020; 49:317–324 [View Article] [PubMed]
     [Google Scholar]
  103. Vanaporn M, Titball RW. Trehalose and bacterial virulence. Virulence 2020; 11:1192–1202 [View Article] [PubMed]
     [Google Scholar]
  104. Li S, Fang L, Liu W, Song T, Zhao F et al. Quantitative proteomic analyses of a pathogenic strain and Its highly passaged attenuated strain of Mycoplasma hyopneumoniae. Biomed Res Int 2019; 2019:4165735 [View Article] [PubMed]
     [Google Scholar]
  105. Moran NA. Microbial minimalism: genome reduction in bacterial pathogens. Cell 2002; 108:583–586 [View Article] [PubMed]
     [Google Scholar]
  106. Albalat R, Cañestro C. Evolution by gene loss. Nat Rev Genet 2016; 17:379–391 [View Article] [PubMed]
     [Google Scholar]
  107. Louwen R, Staals RHJ, Endtz HP, van Baarlen P, van der Oost J. The role of CRISPR-Cas systems in virulence of pathogenic bacteria. Microbiol Mol Biol Rev 2014; 78:74–88 [View Article] [PubMed]
     [Google Scholar]
  108. Wu Q, Cui L, Liu Y, Li R, Dai M et al. CRISPR-Cas systems target endogenous genes to impact bacterial physiology and alter mammalian immune responses. Mol Biomed 2022; 3:22 [View Article] [PubMed]
     [Google Scholar]
  109. Newsom S, Parameshwaran HP, Martin L, Rajan R. The CRISPR-Cas mechanism for adaptive immunity and alternate bacterial functions fuels diverse biotechnologies. Front Cell Infect Microbiol 2021; 10: [View Article]
     [Google Scholar]
  110. Sampson TR, Saroj SD, Llewellyn AC, Tzeng Y-L, Weiss DS. A CRISPR/Cas system mediates bacterial innate immune evasion and virulence. Nature 2013; 497:254–257 [View Article] [PubMed]
     [Google Scholar]
  111. Ma K, Cao Q, Luo S, Wang Z, Liu G et al. cas9 enhances bacterial virulence by repressing the regR transcriptional regulator in Streptococcus agalactiae. Infect Immun 2018; 86:e00552-17 [View Article] [PubMed]
     [Google Scholar]
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Comparative genomic analysis identifies potential adaptive variation in Mycoplasma ovipneumoniae
M Gen 10, 001279 (2024); https://doi.org/10.1099/mgen.0.001279
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