BMC Evolutionary Biology | |
Contrasting evolutionary patterns of spore coat proteins in two Bacillus species groups are linked to a difference in cellular structure | |
Adam Driks1  Hong Qin2  | |
[1] Department of Microbiology and Immunology, Loyola University Medical Center, Maywood, IL 60153, USA;Department of Biology, Spelman College, Atlanta, GA 30314, USA | |
关键词: Phylogenetic profiles; Spore coat; Bacillus; | |
Others : 1085008 DOI : 10.1186/1471-2148-13-261 |
|
received in 2013-03-15, accepted in 2013-11-20, 发布年份 2013 | |
【 摘 要 】
Background
The Bacillus subtilis-group and the Bacillus cereus-group are two well-studied groups of species in the genus Bacillus. Bacteria in this genus can produce a highly resistant cell type, the spore, which is encased in a complex protective protein shell called the coat. Spores in the B. cereus-group contain an additional outer layer, the exosporium, which encircles the coat. The coat in B. subtilis spores possesses inner and outer layers. The aim of this study is to investigate whether differences in the spore structures influenced the divergence of the coat protein genes during the evolution of these two Bacillus species groups.
Results
We designed and implemented a computational framework to compare the evolutionary histories of coat proteins. We curated a list of B. subtilis coat proteins and identified their orthologs in 11 Bacillus species based on phylogenetic congruence. Phylogenetic profiles of these coat proteins show that they can be divided into conserved and labile ones. Coat proteins comprising the B. subtilis inner coat are significantly more conserved than those comprising the outer coat. We then performed genome-wide comparisons of the nonsynonymous/synonymous substitution rate ratio, dN/dS, and found contrasting patterns: Coat proteins have significantly higher dN/dS in the B. subtilis-group genomes, but not in the B. cereus-group genomes. We further corroborated this contrast by examining changes of dN/dS within gene trees, and found that some coat protein gene trees have significantly different dN/dS between the B subtilis-clade and the B. cereus-clade.
Conclusions
Coat proteins in the B. subtilis- and B. cereus-group species are under contrasting selective pressures. We speculate that the absence of the exosporium in the B. subtilis spore coat effectively lifted a structural constraint that has led to relaxed negative selection pressure on the outer coat.
【 授权许可】
2013 Qin and Driks; licensee BioMed Central Ltd.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20150113165948408.pdf | 1291KB | download | |
Figure 7. | 51KB | Image | download |
Figure 6. | 52KB | Image | download |
Figure 5. | 65KB | Image | download |
Figure 4. | 39KB | Image | download |
Figure 3. | 142KB | Image | download |
Figure 2. | 51KB | Image | download |
Figure 1. | 28KB | Image | download |
【 图 表 】
Figure 1.
Figure 2.
Figure 3.
Figure 4.
Figure 5.
Figure 6.
Figure 7.
【 参考文献 】
- [1]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(1):165-170.
- [2]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(3):548-572.
- [3]Losick R, Youngman P, Piggot PJ: Genetics of endospore formation in Bacillus subtilis. Annu Rev Genet 1986, 20:625-669.
- [4]Claus D, Berkeley RCW: Genus Bacillus Cohn 1872. In Bergey’s Manual of Systematic Bacteriology. 2nd edition. Edited by Sneath PHA, Mair NS, Sharpe ME, Holt JG. Baltimore: Williams & Wilkins; 1986:1105-1139.
- [5]Moir A: How do spores germinate? J Appl Microbiol 2006, 101(3):526-530.
- [6]Fritze D: Taxonomy of the genus Bacillus and related genera: the aerobic endospore-forming bacteria. Phytopathology 2004, 94:1245-1248.
- [7]Tourasse NJ, Helgason E, Okstad OA, Hegna IK, Kolsto AB: The Bacillus cereus group: novel aspects of population structure and genome dynamics. J Appl Microbiol 2006, 101(3):579-593.
- [8]Mock M, Fouet A: Anthrax. Annu Rev Microbiol 2001, 55:647-671.
- [9]Stenfors Arnesen LP, Fagerlund A, Granum PE: From soil to gut: Bacillus cereus and its food poisoning toxins. FEMS Microbiol Rev 2008, 32(4):579-606.
- [10]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):1-8.
- [11]Sonenshein AL, Hoch JA, Losick R: Bacillus subtilis and its closest relatives. Washington: American Society for Microbiology; 2002.
- [12]Blackwood KS, Turenne CY, Harmsen D, Kabani AM: Reassessment of sequence-based targets for identification of Bacillus species. J Clin Microbiol 2004, 42(4):1626-1630.
- [13]Driks A: Surface appendages of bacterial spores. Mol Microbiol 2007, 63(3):623-625.
- [14]Henriques AO, Moran CP Jr: Structure, assembly, and function of the spore surface layers. Annu Rev Microbiol 2007, 61:555-588.
- [15]Driks A: Bacillus subtilis spore coat. Microbiol Mol Biol Rev 1999, 63(1):1-20.
- [16]Driks A: Maximum shields: the assembly and function of the bacterial spore coat. Trends Microbiol 2002, 10(6):251-254.
- [17]Driks A, Mallozzi M: Outer structures of the Bacillus anthracis spore. In Bacillus anthracis and Anthrax. Edited by Bergman N. New Jersey: John Wiley & Sons; 2009.
- [18]McKenney PT, Driks A, Eichenberger P: The Bacillus subtilis endospore: assembly and functions of the multilayered coat. Nat Rev Microbiol 2013, 11(1):33-44.
- [19]Chen G, Driks A, Tawfig K, Mallozzi M, Patil S: Bacillus anthracis and Bacillus subtilis Spore surface properties and transport. Colloids Surf B: Biointerfaces 2010, 76(2):512-518.
- [20]Ragkousi K, Eichenberger P, van Ooij C, Setlow P: Identification of a new gene essential for germination of Bacillus subtilis spores with Ca2+-dipicolinate. J Bacteriol 2003, 185(7):2315-2329.
- [21]Riesenman PJ, Nicholson WL: Role of the spore coat layers in Bacillus subtilis spore resistance to hydrogen peroxide, artificial UV-C, UV-B, and solar UV radiation. Appl Environ Microbiol 2000, 66(2):620-626.
- [22]Setlow B, Atluri S, Kitchel R, Koziol-Dube K, Setlow P: Role of dipicolinic acid in resistance and stability of spores of Bacillus subtilis with or without DNA-protective alpha/beta-type small acid-soluble proteins. J Bacteriol 2006, 188(11):3740-3747.
- [23]Behravan J, Chirakkal H, Masson A, Moir A: Mutations in the gerP locus of Bacillus subtilis and Bacillus cereus affect access of germinants to their targets in spores. J Bacteriol 2000, 182(7):1987-1994.
- [24]Setlow P: Spores of Bacillus subtilis: their resistance to and killing by radiation, heat and chemicals. J Appl Microbiol 2006, 101(3):514-525.
- [25]Cohn F: Studies on the biology of the Bacilli. Beiträge zur Biologie der Pflanzen 1876, 2:249-276.
- [26]Koch R: The etiology of anthrax, based on the life history of Bacillus anthracis. Beitr Biol Pflanz 1876, 2:277-310.
- [27]Holt SC, Leadbetter ER: Comparative ultrastructure of selected aerobic spore-forming bacteria: a freeze-etching study. Bacteriol Rev 1969, 33(2):346-378.
- [28]Aronson AI, Fitz-James P: Structure and morphogenesis of the bacterial spore coat. Bacteriol Rev 1976, 40:360-402.
- [29]Traag BA, Driks A, Stragier P, Bitter W, Broussard G, Hatfull G, Chu F, Adams KN, Ramakrishnan L, Losick R: Do mycobacteria produce endospores? Proc Natl Acad Sci U S A 2010, 107(2):878-881.
- [30]Warth AD, Ohye DF, Murrell WG: Location and composition of spore mucopeptide in Bacillus species. J Cell Biol 1963, 16:593-609.
- [31]McKenney PT, Driks A, Eskandarian HA, Grabowski P, Guberman J, Wang KH, Gitai Z, Eichenberger P: A distance-weighted interaction map reveals a previously uncharacterized layer of the Bacillus subtilis spore coat. Curr Biol 2010, 20(10):934-938.
- [32]Hannay CL: The parasporal body of Bacillus laterosporus Laubach. J Biophys Biochem Cytol 1957, 3:1001-1010.
- [33]Vary PS: Prime time for Bacillus megaterium. Microbiology 1994, 140(Pt 5):1001-1013.
- [34]Giorno R, Bozue J, Cote C, Wenzel T, Moody KS, Mallozzi M, Ryan M, Wang R, Zielke R, Maddock JR, et al.: Morphogenesis of the Bacillus anthracis spore. J Bacteriol 2007, 189(3):691-705.
- [35]Kailas L, Terry C, Abbott N, Taylor R, Mullin N, Tzokov SB, Todd SJ, Wallace BA, Hobbs JK, Moir A, et al.: Surface architecture of endospores of the Bacillus cereus/anthracis/thuringiensis family at the subnanometer scale. Proc Natl Acad Sci U S A 2011, 108(38):16014-16019.
- [36]Sylvestre P, Couture-Tosi E, Mock M: Polymorphism in the collagen-like region of the Bacillus anthracis BclA protein leads to variation in exosporium filament length. J Bacteriol 2003, 185(5):1555-1563.
- [37]Sylvestre P, Couture-Tosi E, Mock M: A collagen-like surface glycoprotein is a structural component of the Bacillus anthracis exosporium. Mol Microbiol 2002, 45(1):169-178.
- [38]Daubenspeck JM, Zeng H, Chen P, Dong S, Steichen CT, Krishna NR, Pritchard DG, Turnbough CL Jr: Novel oligosaccharide side chains of the collagen-like region of BclA, the major glycoprotein of the Bacillus anthracis exosporium. J Biol Chem 2004, 279(30):30945-30953.
- [39]Oliva CR, Swiecki MK, Griguer CE, Lisanby MW, Bullard DC, Turnbough CL Jr, Kearney JF: The integrin Mac-1 (CR3) mediates internalization and directs Bacillus anthracis spores into professional phagocytes. Proc Natl Acad Sci U S A 2008, 105:1261-1266.
- [40]Bozue J, Moody KL, Cote CK, Stiles BG, Friedlander AM, Welkos SL, Hale ML: Bacillus anthracis spores of the bclA mutant exhibit increased adherence to epithelial cells, fibroblasts, and endothelial cells but not to macrophages. Infect Immun 2007, 75(9):4498-4505.
- [41]Ball DA, Taylor R, Todd SJ, Redmond C, Couture-Tosi E, Sylvestre P, Moir A, Bullough PA: Structure of the exosporium and sublayers of spores of the Bacillus cereus family revealed by electron crystallography. Mol Microbiol 2008, 68:947-958.
- [42]Driks A: Proteins of the spore core and coat. In Bacillus subtilis and its closest relatives. Edited by Sonenshein AL, Hoch JA, Losick R. Washington, D.C: American Society for Microbiology; 2002:527-536.
- [43]Bielawski JP, Yang Z: Maximum Likelihood Methods for Detecting Adaptive Protein Evolution. In Statistical Methods in Molecular Evolution. Edited by Nielsen R. New York: Springer; 2005:103-124.
- [44]Yang Z: Computational Molecular Evolution. Oxford: Oxford University Press; 2006.
- [45]Gevers D, Cohan FM, Lawrence JG, Spratt BG, Coenye T, Feil EJ, Stackebrandt E, Van de Peer Y, Vandamme P, Thompson FL, et al.: Opinion: Re-evaluating prokaryotic species. Nat Rev Microbiol 2005, 3(9):733-739.
- [46]Priest FG, Barker M, Baillie LW, Holmes EC, Maiden MC: Population structure and evolution of the Bacillus cereus group. J Bacteriol 2004, 186(23):7959-7970.
- [47]Vilas-Boas GT, Peruca AP, Arantes OM: Biology and taxonomy of Bacillus cereus, Bacillus anthracis, and Bacillus thuringiensis. Can J Microbiol 2007, 53(6):673-687.
- [48]Kim H, Hahn M, Grabowski P, McPherson DC, Otte MM, Wang R, Ferguson CC, Eichenberger P, Driks A: The Bacillus subtilis spore coat protein interaction network. Mol Microbiol 2006, 59(2):487-502.
- [49]Eichenberger P, Fujita M, Jensen ST, Conlon EM, Rudner DZ, Wang ST, Ferguson C, Haga K, Sato T, Liu JS, et al.: The program of gene transcription for a single differentiating cell type during sporulation in Bacillus subtilis. PLoS Biol 2004, 2:e328.
- [50]Eichenberger P, Jensen ST, Conlon EM, van Ooij C, Silvaggi J, Gonzalez-Pastor JE, Fujita M, Ben-Yehuda S, Stragier P, Liu JS, et al.: The sigmaE regulon and the identification of additional sporulation genes in Bacillus subtilis. J Mol Biol 2003, 327(5):945-972.
- [51]Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25(17):3389-3402.
- [52]Enright AJ, Van Dongen S, Ouzounis CA: An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res 2002, 30(7):1575-1584.
- [53]Bork P, Dandekar T, Diaz-Lazcoz Y, Eisenhaber F, Huynen M, Yuan Y: Predicting function: from genes to genomes and back. J Mol Biol 1998, 283(4):707-725.
- [54]Tatusov RL, Koonin EV, Lipman DJ: A genomic perspective on protein families. Science 1997, 278(5338):631-637.
- [55]Moreno-Hagelsieb G, Latimer K: Choosing BLAST options for better detection of orthologs as reciprocal best hits. Bioinformatics 2008, 24(3):319-324.
- [56]Fitch WM: Homology a personal view on some of the problems. Trends Genet 2000, 16(5):227-231.
- [57]Li W-H: Molecular Evolution. Sunderland, Massachusetts: Sinauer Associates; 1997.
- [58]Driks A: Overview: development in bacteria: spore formation in Bacillus subtilis. Cell Mol Life Sci 2002, 59(3):389-391.
- [59]Hurst LD: The Ka/Ks ratio: diagnosing the form of sequence evolution. Trends Genet 2002, 18(9):486.
- [60]Yang Z, Nielsen R: Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol 2000, 17(1):32-43.
- [61]Rocha EP, Smith JM, Hurst LD, Holden MT, Cooper JE, Smith NH, Feil EJ: Comparisons of dN/dS are time dependent for closely related bacterial genomes. J Theor Biol 2006, 239(2):226-235.
- [62]Wilke CO, Drummond DA: Signatures of protein biophysics in coding sequence evolution. Curr Opin Struct Biol 2010, 20(3):385-389.
- [63]Salzberg SL, Delcher AL, Kasif S, White O: Microbial gene identification using interpolated Markov models. Nucleic Acids Res 1998, 26(2):544-548.
- [64]Ribosomal Database Project. [https://rdp.cme.msu.edu/ webcite]
- [65]Moszer I, Jones LM, Moreira S, Fabry C, Danchin A: SubtiList: the reference database for the Bacillus subtilis genome. Nucleic Acids Res 2002, 30(1):62-65.
- [66]SubtList. [http://genolist.pasteur.fr/SubtiList/ webcite]
- [67]Kobayashi K, Ehrlich SD, Albertini A, Amati G, Andersen KK, Arnaud M, Asai K, Ashikaga S, Aymerich S, Bessieres P, et al.: Essential Bacillus subtilis genes. Proc Natl Acad Sci U S A 2003, 100(8):4678-4683.
- [68]Priest FG, Kaji DA, Rosato YB, Canhos VP: Characterization of Bacillus thuringiensis and related bacteria by ribosomal RNA gene restriction fragment length polymorphisms. Microbiology 1994, 140(Pt 5):1015-1022.
- [69]Goto K, Omura T, Hara Y, Sadaie Y: Application of the partial 16S rDNA sequence as an index for rapid identification of species in the genus Bacillus. J Gen Appl Microbiol 2000, 46(1):1-8.
- [70]Xu D, Cote JC: Phylogenetic relationships between Bacillus species and related genera inferred from comparison of 3′ end 16S rDNA and 5′ end 16S-23S ITS nucleotide sequences. Int J Syst Evol Microbiol 2003, 53(Pt 3):695-704.
- [71]Cole JR, Chai B, Farris RJ, Wang Q, Kulam-Syed-Mohideen AS, McGarrell DM, Bandela AM, Cardenas E, Garrity GM, Tiedje JM: The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data. Nucleic Acids Res 2007, 35(Database issue):D169-D172.
- [72]Kumar S, Nei M, Dudley J, Tamura K: MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 2008, 9(4):299-306.
- [73]Tamura K, Dudley J, Nei M, Kumar S: MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 2007, 24(8):1596-1599.
- [74]Swofford DL: PAUP*. Phylogennetic Analysis Using Parsimony(* and Other Methods). Version 4. In. Sunderland, Massachusetts: Sinauer Assocates; 2002.
- [75]Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19(12):1572-1574.
- [76]Huelsenbeck JP, Ronquist F: MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 2001, 17(8):754-755.
- [77]Rannala B, Yang Z: Phylogenetic inference using whole genomes. Annu Rev Genomics Hum Genet 2008, 9:217-231.
- [78]Rasko DA, Ravel J, Okstad OA, Helgason E, Cer RZ, Jiang L, Shores KA, Fouts DE, Tourasse NJ, Angiuoli SV, et al.: The genome sequence of Bacillus cereus ATCC 10987 reveals metabolic adaptations and a large plasmid related to Bacillus anthracis pXO1. Nucleic Acids Res 2004, 32(3):977-988.
- [79]Han CS, Xie G, Challacombe JF, Altherr MR, Bhotika SS, Brown N, Bruce D, Campbell CS, Campbell ML, Chen J, et al.: Pathogenomic sequence analysis of Bacillus cereus and Bacillus thuringiensis isolates closely related to Bacillus anthracis. J Bacteriol 2006, 188(9):3382-3390.
- [80]Shimodaira H, Hasegawa M: CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 2001, 17(12):1246-1247.
- [81]R Development Core Team: R: A language and environment for statistical computing. 2009. http://www.R-project.org webcite
- [82]Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al.: Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23(21):2947-2948.
- [83]Stajich JE, Block D, Boulez K, Brenner SE, Chervitz SA, Dagdigian C, Fuellen G, Gilbert JG, Korf I, Lapp H, et al.: The Bioperl toolkit: Perl modules for the life sciences. Genome Res 2002, 12(10):1611-1618.
- [84]Felsenstein J: PHYLIP (Phylogeny inference package) version 3.6. Seattle: Distributed by the author Department of Genome Sciences, University of Washington; 2005.
- [85]Paradis E, Claude J, Strimmer K: APE: analyses of phylogenetics and evolution in R. Bioinformatics 2004, 20:289-290.
- [86]Yang Z: PAML: a program package for phylogenetic analysis by maximum likelihood. CABIOS 1997, 13:555-556.
- [87]Yang Z: Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol Biol Evol 1998, 15(5):568-573.
- [88]Huson DH, Richter DC, Rausch C, Dezulian T, Franz M, Rupp R: Dendroscope: An interactive viewer for large phylogenetic trees. BMC Bioinforma 2007, 8:460. BioMed Central Full Text
- [89]Rice P, Longden I, Bleasby A: EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 2000, 16(6):276-277.
- [90]Linding R, Jensen LJ, Diella F, Bork P, Gibson TJ, Russell RB: Protein disorder prediction: implications for structural proteomics. Structure 2003, 11(11):1453-1459.
- [91]Claverie JM, States D: Information enhancement methods for large scale sequence analysis. Comput Chem 1993, 17:191-201.
- [92]The GitHub repository for this project. https://github.com/hongqin/BacillusSporeCoat webcite