期刊论文详细信息
BMC Research Notes
Evolutionary dynamics of rhomboid proteases in Streptomycetes
Monica Trujillo1  Naydu M Carmona1  Peter A Novick1 
[1] Biological Sciences and Geology Department, Queensborough Community College, City University of New York, Bayside, NY, USA
关键词: Bioinformatics;    S. coelicolor;    Proteases;    Rhomboid proteins;    Streptomyces;   
Others  :  1231982
DOI  :  10.1186/s13104-015-1205-x
 received in 2015-02-19, accepted in 2015-05-08,  发布年份 2015
【 摘 要 】

Background

Proteolytic enzymes are ubiquitous and active in a myriad of biochemical pathways. One type, the rhomboids are intramembrane serine proteases that release their products extracellularly. These proteases are present in all forms of life and their function is not fully understood, although some evidence suggests they participate in cell signaling. Streptomycetes are prolific soil bacteria with diverse physiological and metabolic properties that respond to signals from other cells and from the environment. In the present study, we investigate the evolutionary dynamics of rhomboids in Streptomycetes, as this can shed light into the possible involvement of rhomboids in the complex lifestyles of these bacteria.

Results

Analysis of Streptomyces genomes revealed that they harbor up to five divergent putative rhomboid genes (arbitrarily labeled families A–E), two of which are orthologous to rhomboids previously described in Mycobacteria. Characterization of each of these rhomboid families reveals that each group is distinctive, and has its own evolutionary history. Two of the Streptomyces rhomboid families are highly conserved across all analyzed genomes suggesting they are essential. At least one family has been horizontally transferred, while others have been lost in several genomes. Additionally, the transcription of the four rhomboid genes identified in Streptomyces coelicolor, the model organism of this genus, was verified by reverse transcription.

Conclusions

Using phylogenetic and genomic analysis, this study demonstrates the existence of five distinct families of rhomboid genes in Streptomycetes. Families A and D are present in all nine species analyzed indicating a potentially important role for these genes. The four rhomboids present in S. coelicolor are transcribed suggesting they could participate in cellular metabolism. Future studies are needed to provide insight into the involvement of rhomboids in Streptomyces physiology. We are currently constructing knock out (KO) mutants for each of the rhomboid genes from S. coelicolor and will compare the phenotypes of the KOs to the wild type strain.

【 授权许可】

   
2015 Novick et al.

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【 参考文献 】
  • [1]Bier E, Jan LY, Jan YN: Rhomboid, a gene required for dorsoventral axis establishment and peripheral nervous system development in Drosophila melanogaster. Genes Dev 1990, 4(2):190-203.
  • [2]Urban S, Dickey SW: The rhomboid protease family: a decade of progress on function and mechanism. Genome Biol 2011, 12(10):231. BioMed Central Full Text
  • [3]Vinothkumar KR, Strisovsky K, Andreeva A, Christova Y, Verhelst S, Freeman M: The structural basis for catalysis and substrate specificity of a rhomboid protease. EMBO J 2010, 29(22):3797-3809.
  • [4]Sampathkumar P, Mak MW, Fischer-Witholt SJ, Guigard E, Kay CM: Lemieux MJ (2012) Oligomeric state study of prokaryotic rhomboid proteases. Biochim Biophys Acta 1818, 12:3090-3097.
  • [5]Freeman M: Rhomboid proteases and their biological functions. Annu Rev Genet 2008, 42:191-210.
  • [6]Bergbold N, Lemberg MK: Emerging role of rhomboid family proteins in mammalian biology and disease. Biochim Biophys Acta 2013, 1828(12):2840-2848.
  • [7]Stevenson LG, Strisovsky K, Clemmer KM, Bhatt S, Freeman M, Rather PN: Rhomboid protease AarA mediates quorum-sensing in Providencia stuartii by activating TatA of the twin-arginine translocase. Proc Natl Acad Sci USA 2007, 104(3):1003-1008.
  • [8]Mesak LR, Mesak FM, Dahl MK: Expression of a novel gene, gluP, is essential for normal Bacillus subtilis cell division and contributes to glucose export. BMC Microbiol 2004, 4:13. BioMed Central Full Text
  • [9]Maegawa S, Ito K, Akiyama Y: Proteolytic action of GlpG, a rhomboid protease in the Escherichia coli cytoplasmic membrane. Biochemistry 2005, 44(41):13543-13552.
  • [10]Kateete DP, Okee M, Katabazi FA, Okeng A, Asiimwe J, Boom HW, et al.: Rhomboid homologs in Mycobacteria: insights from phylogeny and genomic analysis. BMC Microbiol 2010, 10:272. BioMed Central Full Text
  • [11]Kateete DP, Katabazi FA, Okeng A, Okee M, Musinguzi C, Asiimwe BB, et al.: Rhomboids of Mycobacteria: characterization using an aarA mutant of Providencia stuartii and gene deletion in Mycobacterium smegmatis. PLoS One 2012, 7(9):e45741.
  • [12]Eritt I, Grafe U, Fleck WF: Inducers of both cytodifferentiation and anthracycline biosynthesis of Streptomyces griseus and their occurrence in actinomycetes and other microorganisms. Z Allg Mikrobiol 1984, 24(1):3-12.
  • [13]Yoshimoto Y, Sawa T, Naganawa H, Sugai T, Takeuchi T, Imoto M: MK800-62F1, a new inhibitor of apoptotic cell death, from Streptomyces diastatochromogenes MK800-62F1. II. Structure elucidation. J Antibiot (Tokyo) 2000, 53(6):575-578.
  • [14]Hayakawa Y, Sasak K, Nagai K, Shin-ya K, Furihata K: Structure of thioviridamide, a novel apoptosis inducer from Streptomyces olivoviridis. J Antibiot (Tokyo) 2006, 59(1):6-10.
  • [15]Hayakawa Y, Sasaki K, Adachi H, Furihata K, Nagai K, Shin-ya K: Thioviridamide, a novel apoptosis inducer in transformed cells from Streptomyces olivoviridis. J Antibiot (Tokyo) 2006, 59(1):1-5.
  • [16]Tomikawa T, Shin-Ya K, Furihata K, Kinoshita T, Miyajima A, Seto H, et al.: Rasfonin, a new apoptosis inducer in ras-dependent cells from Talaromyces sp. J Antibiot (Tokyo) 2000, 53(8):848-850.
  • [17]Trew SJ, Wrigley SK, Pairet L, Sohal J, Shanu-Wilson P, Hayes MA, et al.: Novel streptopyrroles from Streptomyces rimosus with bacterial protein histidine kinase inhibitory and antimicrobial activities. J Antibiot (Tokyo) 2000, 53(1):1-11.
  • [18]Pamboukian CR, Facciotti MC: Production of antitumoral retamycin during fed-batch fermentations of Streptomyces olindensis. Appl Biochem Biotechnol 2004, 112(2):111-122.
  • [19]Craney A, Ozimok C, Pimentel-Elardo SM, Capretta A, Nodwell JR: Chemical perturbation of secondary metabolism demonstrates important links to primary metabolism. Chem Biol 2012, 19(8):1020-1027.
  • [20]Gehring AM, Wang ST, Kearns DB, Storer NY, Losick R: Novel genes that influence development in Streptomyces coelicolor. J Bacteriol 2004, 186(11):3570-3577.
  • [21]McArthur M, Bibb MJ: Manipulating and understanding antibiotic production in Streptomyces coelicolor A3(2) with decoy oligonucleotides. Proc Natl Acad Sci USA 2008, 105(3):1020-1025.
  • [22]Xu W, Huang J, Lin R, Shi J, Cohen SN: Regulation of morphological differentiation in S. coelicolor by RNase III (AbsB) cleavage of mRNA encoding the AdpA transcription factor. Mol Microbiol 2010, 75(3):781-791.
  • [23]Bibb MJ: Regulation of secondary metabolism in Streptomycetes. Curr Opin Microbiol 2005, 8(2):208-215.
  • [24]Ikeda H, Ishikawa J, Hanamoto A, Shinose M, Kikuchi H, Shiba T, et al.: Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nat Biotechnol 2003, 21(5):526-531.
  • [25]Wang XJ, Yan YJ, Zhang B, An J, Wang JJ, Tian J, et al.: Genome sequence of the milbemycin-producing bacterium Streptomyces bingchenggensis. J Bacteriol 2010, 192(17):4526-4527.
  • [26]Barbe V, Bouzon M, Mangenot S, Badet B, Poulain J, Segurens B, et al.: Complete genome sequence of Streptomyces cattleya NRRL 8057, a producer of antibiotics and fluorometabolites. J Bacteriol 2011, 193(18):5055-5056.
  • [27]Bentley SD, Chater KF, Cerdeño-Tárraga AM, Challis GL, Thomson NR, James KD, et al.: Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 2002, 417(6885):141-147.
  • [28]Grubbs KJ, Biedermann PH, Suen G, Adams SM, Moeller JA, Klassen JL, et al.: Genome sequence of Streptomyces griseus strain XylebKG-1, an ambrosia beetle-associated actinomycete. J Bacteriol 2011, 193(11):2890-2891.
  • [29]Wu K, Chung L, Revill WP, Katz L, Reeves CD: The FK520 gene cluster of Streptomyces hygroscopicus var. ascomyceticus (ATCC 14891) contains genes for biosynthesis of unusual polyketide extender units. Gene 2000, 251(1):81-90.
  • [30]Fischbach M, Godfrey P, Ward D, Young S, Zeng Q, Koehrsen M et al (2013) The genome sequence of Streptomyces pristinaespiralis strain ATCC 25486. Unpublished
  • [31]Bignell DR, Seipke RF, Huguet-Tapia JC, Chambers AH, Parry RJ, Loria R: Streptomyces scabies 87–22 contains a coronafacic acid-like biosynthetic cluster that contributes to plant–microbe interactions. Mol Plant Microbe Interact 2010, 23(2):161-175.
  • [32]Fischbach M, Godfrey P, Ward D, Young S, Zeng Q, Koehrsen M et al (2013) The genome sequence of Streptomyces sviceus strain ATCC 29083. Unpublished
  • [33]Markowitz VM, Chen IM, Palaniappan K, Chu K, Szeto E, Grechkin Y, et al.: IMG: the Integrated Microbial Genomes database and comparative analysis system. Nucleic Acids Res 2012, 40(Database issue):D115-D122.
  • [34]Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41:95–98
  • [35]Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, et al.: The Pfam protein families database. Nucleic Acids Res 2012, 40(Database issue):D290-D301.
  • [36]Sonnhammer EL, von Heijne G, Krogh A: A hidden Markov model for predicting transmembrane helices in protein sequences. Proc Int Conf Intell Syst Mol Biol 1998, 6:175-182.
  • [37]Kall L, Krogh A, Sonnhammer EL: A combined transmembrane topology and signal peptide prediction method. J Mol Biol 2004, 338(5):1027-1036.
  • [38]Spyropoulos IC, Liakopoulos TD, Bagos PG, Hamodrakas SJ: TMRPres2D: high quality visual representation of transmembrane protein models. Bioinformatics 2004, 20(17):3258-3260.
  • [39]Crooks GE, Hon G, Chandonia JM, Brenner SE: WebLogo: a sequence logo generator. Genome Res 2004, 14(6):1188-1190.
  • [40]Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Mol Biol 1990, 215(3):403-410.
  • [41]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.
  • [42]Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA (2000) Practical streptomyces genetics. John Innes Foundation
  • [43]Rozen S, Skaletsky H: Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 2000, 132:365-386.
  • [44]Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA (2000) Practical streptomyces genetics. John Innes Foundation
  • [45]Kinch LN, Grishin NV: Bioinformatics perspective on rhomboid intramembrane protease evolution and function. Biochim Biophys Acta 2013, 1828(12):2937-2943.
  • [46]Brooks CL, Lemieux MJ: Untangling structure–function relationships in the rhomboid family of intramembrane proteases. Biochim Biophys Acta 2013, 1828(12):2862-2872.
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