1887

Microbial Genomics logo

Volume 6, Issue 11

Diversity and evolutionary dynamics of spore-coat proteins in spore-forming species of Bacillales Open Access

Abstract

Among members of the Bacillales order, there are several species capable of forming a structure called an endospore. Endospores enable bacteria to survive under unfavourable growth conditions and germinate when environmental conditions are favourable again. Spore-coat proteins are found in a multilayered proteinaceous structure encasing the spore core and the cortex. They are involved in coat assembly, cortex synthesis and germination. Here, we aimed to determine the diversity and evolutionary processes that have influenced spore-coat genes in various spore-forming species of Bacillales using an approach. For this, we used sequence similarity searching algorithms to determine the diversity of coat genes across 161 genomes of Bacillales. The results suggest that among Bacillales, there is a well-conserved core genome, composed mainly by morphogenetic coat proteins and spore-coat proteins involved in germination. However, some spore-coat proteins are taxa-specific. The best-conserved genes among different species may promote adaptation to changeable environmental conditions. Because most of the species harbour complete or almost complete sets of spore-coat genes, we focused on this genus in greater depth. Phylogenetic reconstruction revealed eight monophyletic groups in the genus, of which three are newly discovered. We estimated the selection pressures acting over spore-coat genes in these monophyletic groups using classical and modern approaches and detected horizontal gene transfer (HGT) events, which have been further confirmed by scanning the genomes to find traces of insertion sequences. Although most of the genes are under purifying selection, there are several cases with individual sites evolving under positive selection. Finally, the HGT results confirm that sporulation is an ancestral feature in .

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Bacillales , Bacillus , horizontal gene transfer , morphogenetic coat proteins , positive/purifying selection and Spore-coat proteins
© 2020 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000451
2020-10-14
2024-04-27
Loading full text...

Full text loading...

/deliver/fulltext/mgen/6/11/mgen000451.html?itemId=/content/journal/mgen/10.1099/mgen.0.000451&mimeType=html&fmt=ahah

References

  1. Maayer PD, Aliyu H, Cowan DA. Reorganising the order Bacillales through phylogenomics. Syst Appl Microbiol 2019; 42:178–189 [View Article][PubMed]
     [Google Scholar]
  2. Paul C, Filippidou S, Jamil I, Kooli W, House GL et al. Bacterial spores, from ecology to biotechnology. Adv Appl Microbiol 2019; 106:79–111 [View Article][PubMed]
     [Google Scholar]
  3. Suitso I, Jõgi E, Talpsep E, Naaber P, Lõivukene K et al. Protective effect by Bacillus smithii TBMI12 spores of Salmonella serotype enteritidis in mice. Benef Microbes 2010; 1:37–42 [View Article][PubMed]
     [Google Scholar]
  4. Wells-Bennik MHJ, Eijlander RT, den Besten HMW, Berendsen EM, Warda AK et al. Bacterial spores in food: survival, emergence, and outgrowth. Annu Rev Food Sci Technol 2016; 7:457–482 [View Article]
     [Google Scholar]
  5. Kotiranta A, Lounatmaa K, Haapasalo M. Epidemiology and pathogenesis of Bacillus cereus infections. Microbes Infect 2000; 2:189–198 [View Article][PubMed]
     [Google Scholar]
  6. Mock M, Fouet A. Anthrax. Annu Rev Microbiol 2001; 55:647–671 [View Article][PubMed]
     [Google Scholar]
  7. Stenfors Arnesen LP, Fagerlund A, Granum PE. From soil to gut: Bacillus cereus and its food poisoning toxins. FEMS Microbiol Rev 2008; 32:579–606 [View Article][PubMed]
     [Google Scholar]
  8. Driks A, Eichenberger P. The spore coat. Microbiol Spectr 2016; 4: [View Article]
     [Google Scholar]
  9. Setlow P. Spore resistance properties. Microbiol Spectr 2014b; 2: [View Article][PubMed]
     [Google Scholar]
  10. Beladjal L, Gheysens T, Clegg JS, Amar M, Mertens J. Life from the ashes: survival of dry bacterial spores after very high temperature exposure. Extremophiles 2018; 22:751–759 [View Article][PubMed]
     [Google Scholar]
  11. Klobutcher LA, Ragkousi K, Setlow P. The Bacillus subtilis spore coat provides "eat resistance" during phagocytic predation by the protozoan Tetrahymena thermophila . Proc Natl Acad Sci U S A 2006; 103:165–170 [View Article][PubMed]
     [Google Scholar]
  12. Nicholson WL, Munakata N, Horneck G, Melosh HJ, Setlow P. Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol Mol Biol Rev 2000; 64:548–572 [View Article][PubMed]
     [Google Scholar]
  13. Setlow P, Wang S, Li Y-Q. Germination of spores of the orders Bacillales and Clostridiales . Annu Rev Microbiol 2017; 71:459–477 [View Article][PubMed]
     [Google Scholar]
  14. Moir A, Cooper G. Spore germination. Microbiol Spectr 2015; 3: [View Article][PubMed]
     [Google Scholar]
  15. Setlow P. Germination of spores of Bacillus species: what we know and do not know. J Bacteriol 2014a; 196:1297–1305 [View Article][PubMed]
     [Google Scholar]
  16. McKenney PT, Driks A, Eichenberger P. The Bacillus subtilis endospore: assembly and functions of the multilayered coat. Nat Rev Microbiol 2013; 11:33–44 [View Article][PubMed]
     [Google Scholar]
  17. Henriques AO, Moran CP. Structure, assembly, and function of the spore surface layers. Annu Rev Microbiol 2007; 61:555–588 [View Article][PubMed]
     [Google Scholar]
  18. Waller LN, Fox N, Fox KF, Fox A, Price RL. Ruthenium red staining for ultrastructural visualization of a glycoprotein layer surrounding the spore of Bacillus anthracis and Bacillus subtilis . J Microbiol Methods 2004; 58:23–30 [View Article]
     [Google Scholar]
  19. Bozue JA, Welkos S, Cote CK. The Bacillus anthracis Exosporium: What’s the Big “Hairy” Deal?. Microbiol Spectr 2015; 3: [View Article]
     [Google Scholar]
  20. McKenney PT, Eichenberger P. Dynamics of spore coat morphogenesis in Bacillus subtilis . Mol Microbiol 2012; 83:245–260 [View Article][PubMed]
     [Google Scholar]
  21. Bauer T, Little S, Stöver AG, Driks A. Functional regions of the Bacillus subtilis spore coat morphogenetic protein CotE. J Bacteriol 1999; 181:7043–7051 [View Article][PubMed]
     [Google Scholar]
  22. Ozin AJ, Henriques AO, Yi H, Moran CP. Morphogenetic proteins SpoVID and SafA form a complex during assembly of the Bacillus subtilis spore coat. J Bacteriol 2000; 182:1828–1833 [View Article][PubMed]
     [Google Scholar]
  23. Zilhão R, Naclerio G, Henriques AO, Baccigalupi L, Moran CP et al. Assembly requirements and role of CotH during spore coat formation in Bacillus subtilis . J Bacteriol 1999; 181:2631–2633 [View Article][PubMed]
     [Google Scholar]
  24. Krajčíková D, Forgáč V, Szabo A, Barák I. Exploring the interaction network of the Bacillus subtilis outer coat and crust proteins. Microbiol Res 2017; 204:72–80 [View Article][PubMed]
     [Google Scholar]
  25. McKenney PT, Driks A, Eskandarian HA, Grabowski P, Guberman J et al. A distance-weighted interaction map reveals a previously uncharacterized layer of the Bacillus subtilis spore coat. Curr Biol 2010; 20:934–938 [View Article][PubMed]
     [Google Scholar]
  26. Galperin MY, Mekhedov SL, Puigbo P, Smirnov S, Wolf YI et al. Genomic determinants of sporulation in bacilli and clostridia: towards the minimal set of sporulation-specific genes. Environ Microbiol 2012; 14:2870–2890 [View Article][PubMed]
     [Google Scholar]
  27. Onyenwoke RU, Brill JA, Farahi K, Wiegel J. Sporulation genes in members of the low G+C Gram-type-positive phylogenetic branch (Firmicutes). Arch Microbiol 2004; 182:182–192 [View Article][PubMed]
     [Google Scholar]
  28. Isticato R, Lanzilli M, Petrillo C, Donadio G, Baccigalupi L et al. Bacillus subtilis builds structurally and functionally different spores in response to the temperature of growth. Environ Microbiol 2020; 22:170–182 [View Article][PubMed]
     [Google Scholar]
  29. Zhu B, Stülke J. SubtiWiki in 2018: from genes and proteins to functional network annotation of the model organism Bacillus subtilis . Nucleic Acids Res 2018; 46:D743–D748 [View Article][PubMed]
     [Google Scholar]
  30. Pearson WR. An introduction to sequence similarity (“homology”) searching. Curr Protoc Bioinformatics 2013; 42:3.1.1–3.1.3 [View Article]
     [Google Scholar]
  31. Steinegger M, Söding J. Clustering huge protein sequence sets in linear time. Nat Commun 2018; 9:1–8 [View Article]
     [Google Scholar]
  32. Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M. KEGG as a reference resource for gene and protein annotation. Nucleic Acids Research 2016; 44:D457–462
     [Google Scholar]
  33. Baesman SM, Stolz JF, Kulp TR, Oremland RS. Enrichment and isolation of Bacillus beveridgei sp. nov., a facultative anaerobic haloalkaliphile from Mono Lake, California, that respires oxyanions of tellurium, selenium, and arsenic. Extremophiles 2009; 13:695–705 [View Article][PubMed]
     [Google Scholar]
  34. Carneiro AR, Ramos RTJ, Dall'Agnol H, Pinto AC, de Castro Soares S et al. Genome sequence of Exiguobacterium antarcticum B7, isolated from a biofilm in ginger lake, King George Island, Antarctica. J Bacteriol 2012; 194:6689–6690 [View Article][PubMed]
     [Google Scholar]
  35. Chaudhari NM, Gupta VK, Dutta C. BPGA- an ultra-fast pan-genome analysis pipeline. Sci Rep 2016; 6:1–10 [View Article]
     [Google Scholar]
  36. Lefort V, Longueville J-E, Gascuel O. Sms: smart model selection in PhyML. Mol Biol Evol 2017; 34:2422–2424 [View Article][PubMed]
     [Google Scholar]
  37. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010; 59:307–321 [View Article][PubMed]
     [Google Scholar]
  38. Suchard MA, Lemey P, Baele G, Ayres DL, Drummond AJ et al. Bayesian phylogenetic and phylodynamic data integration using beast 1.10. Virus Evol 2018; 4:vey016 [View Article][PubMed]
     [Google Scholar]
  39. Lartillot N, Philippe H. Computing Bayes factors using thermodynamic integration. Syst Biol 2006; 55:195–207 [View Article][PubMed]
     [Google Scholar]
  40. Xie W, Lewis PO, Fan Y, Kuo L, Chen MH. Improving marginal likelihood estimation for Bayesian phylogenetic model selection. Syst Biol 2011; 60:150–160 [View Article][PubMed]
     [Google Scholar]
  41. Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA. Posterior summarization in Bayesian phylogenetics using tracer 1.7. Syst Biol 2018; 67:901–904 [View Article][PubMed]
     [Google Scholar]
  42. Kass RE, Raftery AE. Bayes factors. J Am Stat Assoc 1995; 90:773–795 [View Article]
     [Google Scholar]
  43. Cock PJA, Antao T, Chang JT, Chapman BA, Cox CJ et al. Biopython: freely available python tools for computational molecular biology and bioinformatics. Bioinformatics 2009; 25:1422–1423 [View Article][PubMed]
     [Google Scholar]
  44. Abascal F, Zardoya R, Telford MJ. TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations. Nucleic Acids Res 2010; 38:W7–W13 [View Article][PubMed]
     [Google Scholar]
  45. Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P et al. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 2017; 34:3299–3302 [View Article][PubMed]
     [Google Scholar]
  46. Carlson CS, Thomas DJ, Eberle MA, Swanson JE, Livingston RJ et al. Genomic regions exhibiting positive selection identified from dense genotype data. Genome Res 2005; 15:1553–1565 [View Article][PubMed]
     [Google Scholar]
  47. Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 1989; 123:585–595
     [Google Scholar]
  48. Castillo JA, Agathos SN. A genome-wide scan for genes under balancing selection in the plant pathogen Ralstonia solanacearum . BMC Evol Biol 2019; 19:123 [View Article][PubMed]
     [Google Scholar]
  49. Murrell B, Weaver S, Smith MD, Wertheim JO, Murrell S et al. Gene-Wide identification of episodic selection. Mol Biol Evol 2015; 32:1365–1371 [View Article][PubMed]
     [Google Scholar]
  50. Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K et al. Detecting individual sites subject to episodic diversifying selection. PLoS Genet 2012; 8:e1002764 [View Article][PubMed]
     [Google Scholar]
  51. Yang Z. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 1997; 13:555–556 [View Article][PubMed]
     [Google Scholar]
  52. Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 2007; 24:1586–1591 [View Article][PubMed]
     [Google Scholar]
  53. Nielsen R, Yang Z. Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 1998; 148:929–936[PubMed]
     [Google Scholar]
  54. Yang Z, Wong WSW, Nielsen R. Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 2005; 22:1107–1118 [View Article][PubMed]
     [Google Scholar]
  55. Yang Z, Nielsen R, Goldman N, Pedersen AM. Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 2000; 155:431–449[PubMed]
     [Google Scholar]
  56. Chen K, Durand D, Farach-Colton M. NOTUNG: a program for dating gene duplications and optimizing gene family trees. J Comput Biol 2000; 7:429–447 [View Article][PubMed]
     [Google Scholar]
  57. Stolzer M, Lai H, Xu M, Sathaye D, Vernot B et al. Inferring duplications, losses, transfers and incomplete lineage sorting with nonbinary species trees. Bioinformatics 2012; 28:i409–i415 [View Article][PubMed]
     [Google Scholar]
  58. Bastian M, Heymann S, Jacomy M. Gephi: an open source software for exploring and manipulating networks. ICWSM 2009; 8:361–362
     [Google Scholar]
  59. Liu M, Li X, Xie Y, Bi D, Sun J et al. Iceberg 2.0: an updated database of bacterial integrative and conjugative elements. Nucleic Acids Res 2019; 47:D660–D665 [View Article][PubMed]
     [Google Scholar]
  60. Soares SC, Geyik H, Ramos RTJ, de Sá PHCG, Barbosa EGV et al. GIPSy: genomic island prediction software. J Biotechnol 2016; 232:2–11 [View Article][PubMed]
     [Google Scholar]
  61. Saggese A, Isticato R, Cangiano G, Ricca E, Baccigalupi L. CotG-like modular proteins are common among spore-forming Bacilli . J Bacteriol 2016; 198:1513–1520 [View Article][PubMed]
     [Google Scholar]
  62. Chen Y-G, Zhang Y-Q, Shi J-X, Xiao H-D, Tang S-K et al. Jeotgalicoccus marinus sp. nov., a marine bacterium isolated from a sea urchin. Int J Syst Evol Microbiol 2009; 59:1625–1629 [View Article][PubMed]
     [Google Scholar]
  63. Ishikawa M, Nakajima K, Itamiya Y, Furukawa S, Yamamoto Y et al. Halolactibacillus halophilus gen. nov., sp. nov. and Halolactibacillus miurensis sp. nov., halophilic and alkaliphilic marine lactic acid bacteria constituting a phylogenetic lineage in Bacillus rRNA group 1. Int J Syst Evol Microbiol 2005; 55:2427–2439 [View Article][PubMed]
     [Google Scholar]
  64. Zhang Y, Li X, Hao Z, Xi R, Cai Y et al. Hydrogen peroxide-resistant CotA and YjqC of Bacillus altitudinis spores are a promising biocatalyst for catalyzing reduction of sinapic acid and sinapine in rapeseed meal. PLoS One 2016; 11:e0158351 [View Article][PubMed]
     [Google Scholar]
  65. Manetsberger J, Ghosh A, Hall EAH, Christie G. Orthologues of Bacillus subtilis spore crust proteins have a structural role in the Bacillus megaterium QM B1551 spore exosporium. Appl Environ Microbiol 2018; 84: [View Article][PubMed]
     [Google Scholar]
  66. Fakhry S, Sorrentini I, Ricca E, De Felice M, Baccigalupi L. Characterization of spore forming Bacilli isolated from the human gastrointestinal tract. J Appl Microbiol 2008; 105:2178–2186 [View Article][PubMed]
     [Google Scholar]
  67. Tam NKM, Uyen NQ, Hong HA, Duc LH, Hoa TT et al. The intesitinal life cycle of Bacillus subtilis and close relatives. J Bacteriol 2006; 188:2692–2700
     [Google Scholar]
  68. Jeyaram K, Romi W, Singh TA, Adewumi GA, Basanti K et al. Distinct differentiation of closely related species of Bacillus subtilis group with industrial importance. J Microbiol Methods 2011; 87:161–164 [View Article][PubMed]
     [Google Scholar]
  69. Rooney AP, Price NPJ, Ehrhardt C, Swezey JL, Bannan JD. Phylogeny and molecular taxonomy of the Bacillus subtilis species complex and description of Bacillus subtilis subsp. inaquosorum subsp. nov. Int J Syst Evol Microbiol 2009; 59:2429–2436 [View Article][PubMed]
     [Google Scholar]
  70. Aronson AI, Shai Y. Why Bacillus thuringiensis insecticidal toxins are so effective: unique features of their mode of action. FEMS Microbiol Lett 2001; 195:1–8 [View Article][PubMed]
     [Google Scholar]
  71. Bosma EF, van de Weijer AHP, Daas MJA, van der Oost J, de Vos WM et al. Isolation and screening of thermophilic Bacilli from compost for electrotransformation and fermentation: characterization of Bacillus smithii ET 138 as a new biocatalyst. Appl Environ Microbiol 2015; 81:1874–1883 [View Article][PubMed]
     [Google Scholar]
  72. Korneli C, David F, Biedendieck R, Jahn D, Wittmann C. Getting the big beast to work--systems biotechnology of Bacillus megaterium for novel high-value proteins. J Biotechnol 2013; 163:87–96 [View Article][PubMed]
     [Google Scholar]
  73. Vary PS, Biedendieck R, Fuerch T, Meinhardt F, Rohde M et al. Bacillus megaterium—From simple soil bacterium to industrial protein production host. Appl Microbiol Biot 2007; 76:957–967
     [Google Scholar]
  74. Takami H, Horikoshi K. Analysis of the genome of an alkaliphilic Bacillus strain from an industrial point of view. Extremophiles 2000; 4:99–108
     [Google Scholar]
  75. Khatri I, Sharma G, Subramanian S. Composite genome sequence of Bacillus clausii, a probiotic commercially available as Enterogermina®, and insights into its probiotic properties. BMC Microbiol 2019; 19:307 [View Article][PubMed]
     [Google Scholar]
  76. Schendel FJ, Bremmon CE, Flickinger MC, Guettler M, Hanson RS. L-lysine production at 50 degrees C by mutants of a newly isolated and characterized methylotrophic Bacillus sp. Appl Environ Microbiol 1990; 56:963–970 [View Article][PubMed]
     [Google Scholar]
  77. Tiago I, Pires C, Mendes V, Morais PV, da Costa MS et al. Bacillus foraminis sp. nov., isolated from a non-saline alkaline groundwater. Int J Syst Evol Microbiol 2006; 56:2571–2574 [View Article]
     [Google Scholar]
  78. Alebouyeh M, Gooran Orimi P, Azimi-Rad M, Tajbakhsh M, Tajeddin E et al. Fatal sepsis by Bacillus circulans in an immunocompromised patient. Iran J Microbiol 2011; 3:156–158[PubMed]
     [Google Scholar]
  79. Croce O, Hugon P, Lagier J-C, Bibi F, Robert C et al. Genome sequence of Bacillus simplex strain P558, isolated from a human fecal sample. Genome Announc 2014; 2:e01241-14 [View Article][PubMed]
     [Google Scholar]
  80. Kuisiene N, Raugalas J, Spröer C, Kroppenstedt RM, Chitavichius D. Bacillus butanolivorans sp. nov., a species with industrial application for the remediation of n-butanol. Int J Syst Evol Microbiol 2008; 58:505–509 [View Article][PubMed]
     [Google Scholar]
  81. Yumoto I, Hirota K, Yamaga S, Nodasaka Y, Kawasaki T et al. Bacillus asahii sp. nov., a novel bacterium isolated from soil with the ability to deodorize the bad smell generated from short-chain fatty acids. Int J Syst Evol Microbiol 2004; 54:1997–2001 [View Article][PubMed]
     [Google Scholar]
  82. Zhaxybayeva O, Doolittle WF. Lateral gene transfer. Curr Biol 2011; 21:R242–R246 [View Article][PubMed]
     [Google Scholar]
  83. Bellanger X, Payot S, Leblond-Bourget N, Guédon G. Conjugative and mobilizable genomic islands in bacteria: evolution and diversity. FEMS Microbiol Rev 2014; 38:720–760 [View Article][PubMed]
     [Google Scholar]
  84. Burrus V, Pavlovic G, Decaris B, Guédon G. Conjugative transposons: the tip of the iceberg. Mol Microbiol 2002; 46:601–610 [View Article][PubMed]
     [Google Scholar]
  85. Galperin MY. Genome diversity of spore-forming Firmicutes . Microbiol Spectr 2013; 1:TBS-0015–2012 [View Article][PubMed]
     [Google Scholar]
  86. McPherson DC, Kim H, Hahn M, Wang R, Grabowski P et al. Characterization of the Bacillus subtilis spore morphogenetic coat protein CotO. J Bacteriol 2005; 187:8278–8290 [View Article][PubMed]
     [Google Scholar]
  87. Zhang J, Fitz-James PC, Aronson AI. Cloning and characterization of a cluster of genes encoding polypeptides present in the insoluble fraction of the spore coat of Bacillus subtilis . J Bacteriol 1993; 175:3757–3766 [View Article][PubMed]
     [Google Scholar]
  88. Ramos-Silva P, Serrano M, Henriques AO. From root to tips: sporulation evolution and specialization in Bacillus subtilis and the intestinal pathogen Clostridioides difficile . Mol Biol Evol 2019; 36:2714–2736 [View Article][PubMed]
     [Google Scholar]
  89. Shuster B, Khemmani M, Abe K, Huang X, Nakaya Y et al. Contributions of crust proteins to spore surface properties in Bacillus subtilis . Mol Microbiol 2019; 111:825–843 [View Article][PubMed]
     [Google Scholar]
  90. Freitas C, Plannic J, Isticato R, Pelosi A, Zilhão R et al. A protein phosphorylation module patterns the Bacillus subtilis spore outer coat. Mol Microbiol 2020; 8: [View Article][PubMed]
     [Google Scholar]
  91. Nguyen KB, Sreelatha A, Durrant ES, Lopez-Garrido J, Muszewska A et al. Phosphorylation of spore coat proteins by a family of atypical protein kinases. Proc Natl Acad Sci U S A 2016; 113:E3482–E3491 [View Article][PubMed]
     [Google Scholar]
  92. Saggese A, Scamardella V, Sirec T, Cangiano G, Isticato R et al. Antagonistic role of CotG and CotH on spore germination and coat formation in Bacillus subtilis . PLoS One 2014; 9:e104900 [View Article][PubMed]
     [Google Scholar]
  93. Krajcíková D, Lukácová M, Müllerová D, Cutting SM, Barák I. Searching for protein-protein interactions within the Bacillus subtilis spore coat. J Bacteriol 2009; 191:3212–3219 [View Article][PubMed]
     [Google Scholar]
  94. Bartels J, Blüher A, López Castellanos S, Richter M, Günther M et al. The Bacillus subtilis endospore crust: protein interaction network, architecture and glycosylation state of a potential glycoprotein layer. Mol Microbiol 2019; 112:1576–1592 [View Article][PubMed]
     [Google Scholar]
  95. Amon JD, Yadav AK, Ramirez-Guadiana FH, Meeske AJ, Cava F et al. SwsB and SafA are required for CwlJ-dependent spore germination in Bacillus subtilis . J Bacteriol 2019; 202: [View Article]
     [Google Scholar]
  96. Henriques AO, Beall BW, Roland K, Moran CP. Characterization of cotJ, a sigma E-controlled operon affecting the polypeptide composition of the coat of Bacillus subtilis spores. J Bacteriol 1995; 177:3394–3406 [View Article][PubMed]
     [Google Scholar]
  97. Seyler RW, Henriques AO, Ozin AJ, Moran CP. Assembly and interactions of cotJ-encoded proteins, constituents of the inner layers of the Bacillus subtilis spore coat. Mol Microbiol 1997; 25:955–966
     [Google Scholar]
  98. Butzin XY, Troiano AJ, Coleman WH, Griffiths KK, Doona CJ et al. Analysis of the effects of a gerP mutation on the germination of spores of Bacillus subtilis . J Bacteriol 2012; 194:5749–5758 [View Article][PubMed]
     [Google Scholar]
  99. Ghosh A, Manton JD, Mustafa AR, Gupta M, Ayuso-Garcia A et al. Proteins encoded by the gerP operon are localized to the inner coat in Bacillus cereus spores and are dependent on GerPA and SafA for assembly. Appl Environ Microbiol 2018; 84: [View Article][PubMed]
     [Google Scholar]
  100. Monroe A, Setlow P. Localization of the transglutaminase cross-linking sites in the Bacillus subtilis spore coat protein GerQ. J Bacteriol 2006; 188:7609–7616 [View Article]
     [Google Scholar]
  101. Ragkousi K, Setlow P. Transglutaminase-mediated cross-linking of GerQ in the coats of Bacillus subtilis spores. J Bacteriol 2004; 186:5567–5575 [View Article][PubMed]
     [Google Scholar]
  102. Fernandes CG, Martins D, Hernandez G, Sousa AL, Freitas C et al. Temporal and spatial regulation of protein cross-linking by the pre-assembled substrates of a Bacillus subtilis spore coat transglutaminase. PLoS Genet 2019; 15:e1007912 [View Article][PubMed]
     [Google Scholar]
  103. Patel S, Gupta RS. A phylogenomic and comparative genomic framework for resolving the polyphyly of the genus Bacillus: Proposal for six new genera of Bacillus species, Peribacillus gen. nov., Cytobacillus gen. nov., Mesobacillus gen. nov., Neobacillus gen. nov., Metabacillus gen. nov. and Alkalihalobacillus gen. nov. Int J Syst Evol Microbiol 2020; 70:406–438 [View Article][PubMed]
     [Google Scholar]
  104. Nunes F, Fernandes C, Freitas C, Marini E, Serrano M et al. SpoVID functions as a non-competitive hub that connects the modules for assembly of the inner and outer spore coat layers in Bacillus subtilis . Mol Microbiol 2018; 110:576–595 [View Article][PubMed]
     [Google Scholar]
  105. Pereira FC, Nunes F, Cruz F, Fernandes C, Isidro AL et al. A LysM domain intervenes in sequential protein-protein and protein-peptidoglycan interactions important for spore coat assembly in Bacillus subtilis . J Bacteriol 2019; 201: [View Article]
     [Google Scholar]
  106. Abhyankar WR, Kamphorst K, Swarge BN, van Veen H, van der Wel NN et al. The influence of sporulation conditions on the spore coat protein composition of Bacillus subtilis spores. Front Microbiol 2016; 7:1636 [View Article][PubMed]
     [Google Scholar]
  107. Aronson A. Regulation of expression of a select group of Bacillus anthracis spore coat proteins. FEMS Microbiol Lett 2018; 365: [View Article][PubMed]
     [Google Scholar]
  108. Ooij Cvan, Eichenberger P, Losick R. Dynamic patterns of subcellular protein localization during spore coat morphogenesis in Bacillus subtilis . J Bacteriol 2004; 186:4441
     [Google Scholar]
  109. Scheeff ED, Axelrod HL, Miller MD, Chiu H-J, Deacon AM et al. Genomics, evolution, and crystal structure of a new family of bacterial spore kinases. Proteins 2010; 78:1470–1482 [View Article][PubMed]
     [Google Scholar]
  110. Tirumalai MR, Rastogi R, Zamani N, Williams EO, Allen S et al. Candidate genes that may be responsible for the unusual resistances exhibited by Bacillus pumilus SAFR-032 spores. Plos One 2013; 8:e66012
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000451
Loading
Diversity and evolutionary dynamics of spore-coat proteins in spore-forming species of Bacillales
M Gen 6, e000451 (2020); https://doi.org/10.1099/mgen.0.000451
/content/journal/mgen/10.1099/mgen.0.000451
/content/journal/mgen/10.1099/mgen.0.000451
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error