devI is an evolutionarily young negative regulator of Myxococcus xanthus development

Journal of Bacteriology

Volumn 197, Issue 7, 2015, Pages 1249-1262

  Rajagopalan, Ramya ^a   Wielgoss, Sébastien ^b   Lippert, Gerardo ^b   Velicer, Gregory J ^b   Kroos, Lee ^a  

^a Michigan State University   (United States)

^b ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CRISPR ASSOCIATED PROTEIN; BACTERIAL DNA; BACTERIAL PROTEIN; STOP CODON;

ARTICLE; BACTERIAL GROWTH; BACTERIUM ISOLATE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CONTROLLED STUDY; GENE DELETION; GENE EXPRESSION; GENE LOCUS; MOLECULAR EVOLUTION; MYXOCOCCUS XANTHUS; NONHUMAN; OPERON; PRIORITY JOURNAL; PROMOTER REGION; RNA INTERFERENCE; SPOROGENESIS; STOP CODON; BACTERIAL SPORE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; PHYSIOLOGY;

MYXOCOCCUS XANTHUS;

BACTERIAL PROTEINS; CODON, TERMINATOR; DNA, BACTERIAL; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, BACTERIAL; MUTATION; MYXOCOCCUS XANTHUS; OPERON; SPORES, BACTERIAL;

EID: 84924717658     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.02542-14     Document Type: Article

References (81)

1. Velicer GJ, Mendes-Soares H, Wielgloss S. 2014. Whence comes social diversity? Ecological and evolutionary analysis of the myxobacteria, p 1-29. In Yang Z, Higgs P (ed), Myxobacteria: genomics, cellular and molecular biology. Caister Academic Press, Norfolk, United Kingdom.
2. Munoz-Dorado J, Higgs P, Elias-Arnanz M. 2014. Abundance and complexity of signaling mechanisms in myxobacteria, p 127-149. In Yang Z, Higgs P (ed), Myxobacteria: genomics, cellular and molecular biology. Caister Academic Press, Norfolk, United Kingdom.
3. Kaiser D, Robinson M, Kroos L. 2010. Myxobacteria, polarity, and multicellular morphogenesis. Cold Spring Harb Perspect Biol 2:a000380. http://dx.doi.org/10.1101/cshperspect.a000380.
4. Rajagopalan R, Sarwar Z, Garza AG, Kroos L. 2014. Developmental gene regulation, p 105-126. In Yang Z, Higgs P (ed), Myxobacteria: genomics, cellular and molecular biology. Caister Academic Press, Norfolk, United Kingdom.
5. Higgs P, Hartzell PL, Holkenbrink C, Hoiczyk E. 2014. Myxococcus xanthus vegetative and developmental cell heterogeneity, p 51-77. In Yang Z, Higgs P (ed), Myxobacteria: genomics, cellular and molecular biology. Caister Academic Press, Norfolk, United Kingdom.
6. Rajagopalan R, Kroos L. 2014. Nutrient-regulated proteolysis of MrpC halts expression of genes important for commitment to sporulation during Myxococcus xanthus development. J Bacteriol 196:2736-2747. http://dx.doi.org/10.1128/JB.01692-14.
7. Kuner JM, Kaiser D. 1982. Fruiting body morphogenesis in submerged cultures of Myxococcus xanthus. J Bacteriol 151:458-461.
8. Kroos L, Kuspa A, Kaiser D. 1986. A global analysis of developmentally regulated genes in Myxococcus xanthus. Dev Biol 117:252-266. http://dx.doi.org/10.1016/0012-1606(86)90368-4.
9. Kroos L, Kuspa A, Kaiser D. 1990. Defects in fruiting body development caused by Tn5 lac insertions in Myxococcus xanthus. J Bacteriol 172:484-487.
10. Thony-Meyer L, Kaiser D. 1993. devRS, an autoregulated and essential genetic locus for fruiting body development in Myxococcus xanthus. J Bacteriol 175:7450-7462.
11. Boysen A, Ellehauge E, Julien B, Sogaard-Andersen L. 2002. The DevT protein stimulates synthesis of FruA, a signal transduction protein required for fruiting body morphogenesis in Myxococcus xanthus. J Bacteriol 184:1540-1546. http://dx.doi.org/10.1128/JB.184.6.1540-1546.2002.
12. Viswanathan P, Murphy K, Julien B, Garza AG, Kroos L. 2007. Regulation of dev, an operon that includes genes essential for Myxococcus xanthus development and CRISPR-associated genes and repeats. J Bacteriol 189:3738-3750. http://dx.doi.org/10.1128/JB.00187-07.
13. Karginov FV, Hannon GJ. 2010. The CRISPR system: small RNA-guided defense in bacteria and archaea. Mol Cell 37:7-19. http://dx.doi.org/10.1016/j.molcel.2009.12.033.
14. Licking E, Gorski L, Kaiser D. 2000. A common step for changing cell shape in fruiting body and starvation-independent sporulation of Myxococcus xanthus. J Bacteriol 182:3553-3558. http://dx.doi.org/10.1128/JB.182.12.3553-3558.2000.
15. Muller FD, Schink CW, Hoiczyk E, Cserti E, Higgs PI. 2012. Spore formation in Myxococcus xanthus is tied to cytoskeleton functions and polysaccharide spore coat deposition. Mol Microbiol 83:486-505. http://dx.doi.org/10.1111/j.1365-2958.2011.07944.x.
16. Muller FD, Treuner-Lange A, Heider J, Huntley SM, Higgs PI. 2010. Global transcriptome analysis of spore formation in Myxococcus xanthus reveals a locus necessary for cell differentiation. BMC Genomics 11:264. http://dx.doi.org/10.1186/1471-2164-11-264.
17. Viswanathan P, Ueki T, Inouye S, Kroos L. 2007. Combinatorial regulation of genes essential for Myxococcus xanthus development involves a response regulator and a LysR-type regulator. Proc Natl Acad Sci USA 104:7969-7974. http://dx.doi.org/10.1073/pnas.0701569104.
18. Campbell A, Viswanathan P, Barrett T, Son B, Saha S, Kroos L. 2015. Combinatorial regulation of the dev operon by MrpC2 and FruA during Myxococcus xanthus development. J Bacteriol 197:240-251. http://dx.doi.org/10.1128/JB.02310-14.
19. Lee J, Son B, Viswanathan P, Luethy P, Kroos L. 2011. Combinatorial regulation of fmgD by MrpC2 and FruA during Myxococcus xanthus development. J Bacteriol 193:1681-1689. http://dx.doi.org/10.1128/JB.01541-10.
20. Mittal S, Kroos L. 2009. A combination of unusual transcription factors binds cooperatively to control Myxococcus xanthus developmental gene expression. Proc Natl Acad Sci USA 106:1965-1970. http://dx.doi.org/10.1073/pnas.0808516106.
21. Mittal S, Kroos L. 2009. Combinatorial regulation by a novel arrangement of FruA and MrpC2 transcription factors during Myxococcus xanthus development. J Bacteriol 191:2753-2763. http://dx.doi.org/10.1128/JB.01818-08.
22. Son B, Liu Y, Kroos L. 2011. Combinatorial regulation by MrpC2 and FruA involves three sites in the fmgE promoter region during Myxococcus xanthus development. J Bacteriol 193:2756-2766. http://dx.doi.org/10.1128/JB.00205-11.
23. Kroos L, Kaiser D. 1987. Expression of many developmentally regulated genes in Myxococcus depends on a sequence of cell interactions. Genes Dev 1:840-854. http://dx.doi.org/10.1101/gad.1.8.840.
24. Brandner JP, Kroos L. 1998. Identification of the ω4400 regulatory region, a developmental promoter of Myxococcus xanthus. J Bacteriol 180: 1995-2004.
25. Fisseha M, Biran D, Kroos L. 1999. Identification of the ω4499 regulatory region controlling developmental expression of a Myxococcus xanthus cytochrome P-450 system. J Bacteriol 181:5467-5475.
26. Fisseha M, Gloudemans M, Gill R, Kroos L. 1996. Characterization of the regulatory region of a cell interaction-dependent gene in Myxococcus xanthus. J Bacteriol 178:2539-2550.
27. Loconto J, Viswanathan P, Nowak SJ, Gloudemans M, Kroos L. 2005. Identification of the ω4406 regulatory region, a developmental promoter of Myxococcus xanthus, and a DNA segment responsible for chromosomal position-dependent inhibition of gene expression. J Bacteriol 187:4149-4162. http://dx.doi.org/10.1128/JB.187.12.4149-4162.2005.
28. Kim SK, Kaiser D. 1990. C-factor: a cell-cell signaling protein required for fruiting body morphogenesis of M. xanthus. Cell 61:19-26. http://dx.doi.org/10.1016/0092-8674(90)90211-V.
29. Kim SK, Kaiser D. 1990. Purification and properties of Myxococcus xanthus C-factor, an intercellular signaling protein. Proc Natl Acad Sci USA 87:3635-3639. http://dx.doi.org/10.1073/pnas.87.10.3635.
30. Shimkets LJ, Rafiee H. 1990. CsgA, an extracellular protein essential for Myxococcus xanthus development. J Bacteriol 172:5299-5306.
31. Kruse T, Lobedanz S, Berthelsen NM, Sogaard-Andersen L. 2001. C-signal: a cell surface-associated morphogen that induces and coordinates multicellular fruiting body morphogenesis and sporulation in Myxococcus xanthus. Mol Microbiol 40:156-168. http://dx.doi.org/10.1046/j.1365-2958.2001.02365.x.
32. Lobedanz S, Sogaard-Andersen L. 2003. Identification of the C-signal, a contact-dependent morphogen coordinating multiple developmental responses in Myxococcus xanthus. Genes Dev 17:2151-2161. http://dx.doi.org/10.1101/gad.274203.
33. Konovalova A, Lobach S, Sogaard-Andersen L. 2012. A RelA-dependent two-tiered regulated proteolysis cascade controls synthesis of a contactdependent intercellular signal in Myxococcus xanthus. Mol Microbiol 84: 260-275. http://dx.doi.org/10.1111/j.1365-2958.2012.08020.x.
34. Rolbetzki A, Ammon M, Jakovljevic V, Konovalova A, Sogaard-Andersen L. 2008. Regulated secretion of a protease activates intercellular signaling during fruiting body formation in M. xanthus. Dev Cell 15:627-634. http://dx.doi.org/10.1016/j.devcel.2008.08.002.
35. Kim SK, Kaiser D. 1990. Cell motility is required for the transmission of C-factor, an intercellular signal that coordinates fruiting body morphogenesis of Myxococcus xanthus. Genes Dev 4:896-905. http://dx.doi.org/10.1101/gad.4.6.896.
36. Kim SK, Kaiser D. 1990. Cell alignment required in differentiation of Myxococcus xanthus. Science 249:926-928. http://dx.doi.org/10.1126/science.2118274.
37. Kroos L, Hartzell P, Stephens K, Kaiser D. 1988. A link between cell movement and gene expression argues that motility is required for cell-cell signaling during fruiting body development. Genes Dev 2:1677-1685. http://dx.doi.org/10.1101/gad.2.12a.1677.
38. Sager B, Kaiser D. 1994. Intercellular C-signaling and the traveling waves of Myxococcus. Genes Dev 8:2793-2804. http://dx.doi.org/10.1101/gad.8.23.2793.
39. Ellehauge E, Norregaard-Madsen M, Sogaard-Andersen L. 1998. The FruA signal transduction protein provides a checkpoint for the temporal co-ordination of intercellular signals in Myxococcus xanthus development. Mol Microbiol 30:807-817. http://dx.doi.org/10.1046/j.1365-2958.1998.01113.x.
40. Ogawa M, Fujitani S, Mao X, Inouye S, Komano T. 1996. FruA, a putative transcription factor essential for the development of Myxococcus xanthus. Mol Microbiol 22:757-767. http://dx.doi.org/10.1046/j.1365-2958.1996.d01-1725.x.
41. Sager B, Kaiser D. 1993. Two cell-density domains within the Myxococcus xanthus fruiting body. Proc Natl Acad Sci USA 90:3690-3694. http://dx.doi.org/10.1073/pnas.90.8.3690.
42. Jelsbak L, Sogaard-Andersen L. 2002. Pattern formation by a cell surfaceassociated morphogen in Myxococcus xanthus. Proc Natl Acad Sci USA 99:2032-2037. http://dx.doi.org/10.1073/pnas.042535699.
43. Julien B, Kaiser AD, Garza A. 2000. Spatial control of cell differentiation in Myxococcus xanthus. Proc Natl Acad Sci USA 97:9098-9103. http://dx.doi.org/10.1073/pnas.97.16.9098.
44. Sager B, Kaiser D. 1993. Spatial restriction of cellular differentiation. Genes Dev 7:1645-1653. http://dx.doi.org/10.1101/gad.7.9.1645.
45. Nariya H, Inouye S. 2006. A protein Ser/Thr kinase cascade negatively regulates the DNA-binding activity of MrpC, a smaller form of which may be necessary for the Myxococcus xanthus development. Mol Microbiol 60:1205-1217. http://dx.doi.org/10.1111/j.1365-2958.2006.05178.x.
46. Higgs PI, Jagadeesan S, Mann P, Zusman DR. 2008. EspA, an orphan hybrid histidine protein kinase, regulates the timing of expression of key developmental proteins of Myxococcus xanthus. J Bacteriol 190:4416-4426. http://dx.doi.org/10.1128/JB.00265-08.
47. Nariya H, Inouye S. 2005. Identification of a protein Ser/Thr kinase cascade that regulates essential transcriptional activators in Myxococcus xanthus development. Mol Microbiol 58:367-379. http://dx.doi.org/10.1111/j.1365-2958.2005.04826.x.
48. Fiegna F, Velicer GJ. 2005. Exploitative and hierarchical antagonism in a cooperative bacterium. PLoS Biol 3:e370. http://dx.doi.org/10.1371/journal.pbio.0030370.
49. - defect. Mol Microbiol 15:483-494. http://dx.doi.org/10.1111/j.1365-2958.1995.tb02262.x.
50. Ueki T, Inouye S, Inouye M. 1996. Positive-negative KG cassettes for construction of multi-gene deletions using a single drug marker. Gene 183:153-157. http://dx.doi.org/10.1016/S0378-1119(96)00546-X.
51. Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114-2120. http://dx.doi.org/10.1093/bioinformatics/btu170.
52. Li ZF, Li X, Liu H, Liu X, Han K, Wu ZH, Hu W, Li FF, Li YZ. 2011. Genome sequence of the halotolerant marine bacterium Myxococcus fulvus HW-1. J Bacteriol 193:5015-5016. http://dx.doi.org/10.1128/JB.05516-11.
53. Goldman BS, Nierman WC, Kaiser D, Slater SC, Durkin AS, Eisen J, Ronning CM, Barbazuk WB, Blanchard M, Field C, Halling C, Hinkle G, Iartchuk O, Kim HS, Mackenzie C, Madupu R, Miller N, Shvartsbeyn A, Sullivan SA, Vaudin M, Wiegand R, Kaplan HB. 2006. Evolution of sensory complexity recorded in a myxobacterial genome. Proc Natl Acad Sci USA 103:15200-15205. http://dx.doi.org/10.1073/pnas.0607335103.
54. Bertels F, Silander OK, Pachkov M, Rainey PB, van Nimwegen E. 2014. Automated reconstruction of whole-genome phylogenies from shortsequence reads. Mol Biol Evol 31:1077-1088. http://dx.doi.org/10.1093/molbev/msu088.
55. Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312-1313. http://dx.doi.org/10.1093/bioinformatics/btu033.
56. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA. 2012. SPAdes: a new genome assembly algorithm and its applications to singlecell sequencing. J Comput Biol 19:455-477. http://dx.doi.org/10.1089/cmb.2012.0021.
57. Deatherage DE, Barrick JE. 2014. Identification of mutations in laboratory-evolved microbes from next-generation sequencing data using breseq. Methods Mol Biol 1151:165-188. http://dx.doi.org/10.1007/978-1-4939-0554-6_12.
58. Gurevich A, Saveliev V, Vyahhi N, Tesler G. 2013. QUAST: quality assessment tool for genome assemblies. Bioinformatics 29:1072-1075. http://dx.doi.org/10.1093/bioinformatics/btt086.
59. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30: 2725-2729. http://dx.doi.org/10.1093/molbev/mst197.
60. Kadam SV, Velicer GJ. 2006. Variable patterns of density-dependent survival in social bacteria. Behav Ecol 17:833-838. http://dx.doi.org/10.1093/beheco/arl018.
61. Kraemer SA, Velicer GJ. 2011. Endemic social diversity within natural kin groups of a cooperative bacterium. Proc Natl Acad Sci USA 108:10823-10830. http://dx.doi.org/10.1073/pnas.1100307108.
62. Konovalova A, Sogaard-Andersen L, Kroos L. 2014. Regulated proteolysis in bacterial development. FEMS Microbiol Rev 38:493-522. http://dx.doi.org/10.1111/1574-6976.12050.
63. Huntley S, Hamann N, Wegener-Feldbrugge S, Treuner-Lange A, Kube M, Reinhardt R, Klages S, Muller R, Ronning CM, Nierman WC, Sogaard-Andersen L. 2011. Comparative genomic analysis of fruiting body formation in Myxococcales. Mol Biol Evol 28:1083-1097. http://dx.doi.org/10.1093/molbev/msq292.
64. Shimkets LJ, Dworkin M, Reichenbach H. 2006. The myxobacteria, p 31-115. In Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (ed), The prokaryotes. Springer, New York, NY.
65. Huntley S, Wuichet K, Sogaard-Andersen L. 2014. Genome evolution and content in the myxobacteria, p 30-50. In Yang Z, Higgs P (ed), Myxobacteria: genomics, cellular and molecular biology. Caister Academic Press, Norfolk, United Kingdom.
66. Fiegna F, Yu YT, Kadam SV, Velicer GJ. 2006. Evolution of an obligate social cheater to a superior cooperator. Nature 441:310-314. http://dx.doi.org/10.1038/nature04677.
67. Yu YT, Yuan X, Velicer GJ. 2010. Adaptive evolution of an sRNA that controls Myxococcus development. Science 328:993. http://dx.doi.org/10.1126/science.1187200.
68. Hinman VF, Davidson EH. 2007. Evolutionary plasticity of developmental gene regulatory network architecture. Proc Natl Acad Sci USA 104: 19404-19409. http://dx.doi.org/10.1073/pnas.0709994104.
69. van der Oost J, Westra ER, Jackson RN, Wiedenheft B. 2014. Unravelling the structural and mechanistic basis of CRISPR-Cas systems. Nat Rev Microbiol 12:479-492. http://dx.doi.org/10.1038/nrmicro3279.
70. Makarova KS, Haft DH, Barrangou R, Brouns SJ, Charpentier E, Horvath P, Moineau S, Mojica FJ, Wolf YI, Yakunin AF, van der Oost J, Koonin EV. 2011. Evolution and classification of the CRISPRCas systems. Nat Rev Microbiol 9:467-477. http://dx.doi.org/10.1038/nrmicro2577.
71. Makarova KS, Aravind L, Wolf YI, Koonin EV. 2011. Unification of Cas protein families and a simple scenario for the origin and evolution of CRISPR-Cas systems. Biol Direct 6:38. http://dx.doi.org/10.1186/1745-6150-6-38.
72. Bikard D, Marraffini LA. 2013. Control of gene expression by CRISPRCas systems. F1000Prime Rep 5:47. http://dx.doi.org/10.12703/P5-47.
73. Sampson TR, Weiss DS. 2013. Alternative roles for CRISPR/Cas systems in bacterial pathogenesis. PLoS Pathog 9:e1003621. http://dx.doi.org/10.1371/journal.ppat.1003621.
74. Hale CR, Majumdar S, Elmore J, Pfister N, Compton M, Olson S, Resch AM, Glover CV, III, Graveley BR, Terns RM, Terns MP. 2012. Essential features and rational design of CRISPR RNAs that function with the Cas RAMP module complex to cleave RNAs. Mol Cell 45:292-302. http://dx.doi.org/10.1016/j.molcel.2011.10.023.
75. Zhang J, Rouillon C, Kerou M, Reeks J, Brugger K, Graham S, Reimann J, Cannone G, Liu H, Albers SV, Naismith JH, Spagnolo L, White MF. 2012. Structure and mechanism of the CMR complex for CRISPRmediated antiviral immunity. Mol Cell 45:303-313. http://dx.doi.org/10.1016/j.molcel.2011.12.013.
76. Storz G, Wolf YI, Ramamurthi KS. 2014. Small proteins can no longer be ignored. Annu Rev Biochem 83:753-777. http://dx.doi.org/10.1146/annurev-biochem-070611-102400.
77. Levin PA, Fan N, Ricca E, Driks A, Losick R, Cutting S. 1993. An unusually small gene required for sporulation by Bacillus subtilis. Mol Microbiol 9:761-771. http://dx.doi.org/10.1111/j.1365-2958.1993.tb01736.x.
78. van Ooij C, Losick R. 2003. Subcellular localization of a small sporulation protein in Bacillus subtilis. J Bacteriol 185:1391-1398. http://dx.doi.org/10.1128/JB.185.4.1391-1398.2003.
79. Ramamurthi KS, Clapham KR, Losick R. 2006. Peptide anchoring spore coat assembly to the outer forespore membrane in Bacillus subtilis. Mol Microbiol 62:1547-1557. http://dx.doi.org/10.1111/j.1365-2958.2006.05468.x.
80. Ramamurthi KS, Lecuyer S, Stone HA, Losick R. 2009. Geometric cue for protein localization in a bacterium. Science 323:1354-1357. http://dx.doi.org/10.1126/science.1169218.
81. Ebmeier SE, Tan IS, Clapham KR, Ramamurthi KS. 2012. Small proteins link coat and cortex assembly during sporulation in Bacillus subtilis. Mol Microbiol 84:682-696. http://dx.doi.org/10.1111/j.1365-2958.2012.08052.x.