Differential gene expression in bacterial symbionts from loliginid squids demonstrates variation between mutualistic and environmental niches

Environmental Microbiology Reports

Volumn 2, Issue 4, 2010, Pages 514-523

  Guerrero Ferreira, Ricardo C ^a,b   Nishiguchi, Michele K ^a  

^a NEW MEXICO STATE UNIVERSITY   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); CEPHALOPODA; LOLIGINIDAE; MOLLUSCA; PROTEOBACTERIA; SEPIOLIDA; VIBRIO;

EID: 78649751227     PISSN: None     EISSN: 17582229     Source Type: Journal    
DOI: 10.1111/j.1758-2229.2009.00077.x     Document Type: Article

References (65)

1. Actis, L.A., Fish, W., Crosa, J.H., Kellerman, K., Ellenberger, S.R., Hauser, F.M., and Sanders-Loehr, J. (1986) Characterization of anguibactin, a novel siderophore from Vibrio anguillarum 775 (pJM1). J Bacteriol 167: 57-65.
2. Aeckersberg, F., Lupp, C., Feliciano, B., and Ruby, E.G. (2001) Vibrio fischeri outer membrane protein ompU plays a role in normal symbiotic colonization. J Bacteriol 183: 6590-6597.
3. Alexeyev, D.O. (1992) The systematic position of bioluminescent squids of the family Loliginidae (Cephalopoda: Myopsida). Zool Zhurnal 71: 12-23.
4. Anderson, F.E. (2000) Phylogenetic relationships among loliginid squids (Cephalopoda: Myopsida) based on analyses of mulitiple data sets. Zool J Linnean Soc 130: 603-633.
5. Ariyakumar, D.S. (2007) Genetic factors regulating the symbiosis between sepiolid squids (Cephalopoda: Sepiolidae) and their Vibrio symbionts. Masters Thesis. New Mexico State University.
6. Ariyakumar, D.S., and Nishiguchi, M.K. (2009) Characterization of two host specific genes, mannose sensitive hemag-glutinin (mshA) and uridyl phosphate dehydrogenase (UDPDH) that are involved in the Vibrio fischeri-Euprymna tasmanica mutualism. FEMS Microbiol Lett 299: 65-73.
7. Aznar, R., and Alcaide, E. (1992) Siderophores and related outer membrane proteins produced by pseudomonads isolated from eels and freshwater. FEMS Microbiol Lett 98: 269-275.
8. Bagg, A., and Neilands, J.B. (1987) Molecular mechanisms of regulation of siderophore-mediated iron assimilation. Microbiol Rev 51: 509-518.
9. Bassler, B., Clifton, S.W., Fulton, L., Delehaunty, K., Fronick, C., Harrison, M., et al. (2007) The Vibrio harveyi Genome Sequencing Project. Bethesda, MD, USA: Genetics, Genome Sequencing Center, National Center for Biotechnology Information, NIH.
10. Bassler, B.L. (1999) How bacteria talk to each other: regulation of gene expression by quorum sensing. Curr Opin Microbiol 2: 582-587.
11. Bassler, B.L., Gibbons, P.J., Yu, C., and Roseman, S. (1991) Chitin utilization by marine bacteria. Chemotaxis to chitin oligosaccharides by Vibrio furnissii. J Biol Chem 266: 24268-24275.
12. Camilli, A., and Mekalanos, J.J. (1995) Use of recombinase gene fusions to identify Vibrio cholerae genes induced during infection. Mol Microbiol 18: 671-683.
13. Chotiyaputta, C., Nootmorn, P., and Jirapunpipat, K. (2002) Review of cephalopod fishery production and long term changes in fish communities in the Gulf of Thailand. Bull Mar Sci 71: 223-238.
14. Dai, J.-H., Lee, Y-S., and Wong, H.-D. (1992) Effects of iron limitation of production of a siderophore, outer membrane proteins, and hemolysin and on hydrophobicity, cell adherance, and lethality for mice of Vibrio parahaemolyticus. Infect Immun 60: 2952-2956.
15. Daigle, F., Graham, J.E., and Curtiss R., III (2001) Identification of Salmonella typhi genes expressed within macrophages by selective capture of transcribed sequences (SCOTS). Mol Microbiol 41: 1211-1222.
16. Davidson, S.K., Koropatnick, T.A., Kossmehl, R., Sycuro, L., and McFall-Ngai, M.J. (2004) NO means 'yes' in the squid-vibrio symbiosis: nitric oxide (NO) during the initial stages of a beneficial association. Cell Microbiol 6: 1139-1151.
17. Dozois, C.M., Daigle, F., and Curtiss, R., 3rd (2003) Identification of pathogen-specific and conserved genes expressed in vivo by an avian pathogenic Escherichia coli strain. Proc Natl Acad Sci USA 100: 247-252.
18. Dunlap, P.V., Davis, K.M., Tomiyama, S., Fujino, M., and Fukui, A. (2008) Developmental and microbiological analysis of the inception of bioluminescent symbiosis in the marine fish Nuchequula nuchalis (Perciformes: Leiognathidae). Appl Environ Microbiol 74: 7471-7481.
19. Edwards, U., Rogall, T., Blocker, H., Emde, M., and Bottger, E.C. (1989) Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res 17: 7843-7853.
20. Faruque, S.M., Nair, G.B., and Mekalanos, J.J. (2004) Genetics of stress adaptation and virulence in toxigenic Vibrio cholerae. DNA Cell Biol 23: 723-741.
21. Faucher, S.P., Porwollik, S., Dozois, C.M., McClelland, M., and Daigle, F. (2006) Transcriptome of Salmonella enterica serovar Typhi within macrophages revealed through the selective capture of transcribed sequences. Proc Natl Acad Sci USA 103: 1906-1911.
22. Gottschalk, G. (1986) Bacterial Metabolism. New York, NY, USA: Springer
23. Graf, J., and Ruby, E.G. (1998) Host-derived amino acids support the proliferation of symbiotic bacteria. Proc Natl Acad Sci USA 95: 1818-1822.
24. Graf, J., and Ruby, E.G. (2000) Novel effects of a transposon insertion in the Vibrio fischeri glnD gene: defects in iron uptake and symbiotic persistence in addition to nitrogen utilization. Mol Microbiol 37: 168-179.
25. Graham, J.E., and Clark-Curtiss, J.E. (1999) Identification of Mycobacterium tuberculosis RNA's synthesized in response to phagocytosis by human macrophages by selective capture of transcribed sequences (SCOTS). Proc Natl Acad Sci USA 96: 11554-11559.
26. Graham, J.E., Peek, R.M.J., Krishna, U., and Cover, T.L. (2002) Global analysis of Helicobacter pylori gene expression in human gastric mucosa. Gastroenterology 123: 1637-1648.
27. Graham, J.E., and Clark-Curtiss, J.E. (2000) Identifying Mycobacterium tuberculosis virulence determinants - new technologies for a difficult problem: response. Trends Microbiol 8: 100.
28. Guerrero-Ferreira, R.C., and Nishiguchi, M.K. (2007) Biodiversity among luminescent symbionts from squid of the genera Uroteuthis, Loliolus and Euprymna (Mollusca: Cephalopoda). Cladistics 23: 497-506.
29. Heithoff, D.M., Conner, C.P., Hanna, P.C., Julio, S.M., Hentschel, U., and Mahan, M.J. (1997) Bacterial infection as assessed by in vivo gene expression. Proc Natl Acad Sci USA 94: 934-939.
30. Heithoff, D.M., Sinsheimer, R.L., Low, D.A., and Mahan, M.J. (1999) An essential role for DNA adenine methylation in bacterial virulence. Science 284: 967-970.
31. Henderson, D.P., and Payne, S.M. (1994) Vibrio cholerae iron transport systems: roles of heme and siderophore iron transport in virulence and identification of a gene associated with multiple iron transport systems. Infect Immun 62: 5120-5125.
32. Hou, J.Y., Graham, J.E., and Clark-Curtiss, J.E. (2002) Mycobacterium avium genes expressed during growth in human macrophages detected by selective capture of transcribed sequences (SCOTS). Infect Immun 70: 3714-3726.
33. Jones, B.W., and Nishiguchi, M.K. (2004) Counterillumination in the bobtail squid, Euprymna scolopes Berry (Mollusca: Cephalopoda). Mar Biol 144: 1151-1155.
34. Jones, B.W., and Nishiguchi, M.K. (2006) Differentially expressed genes reveal adaptations between free-living and symbiotic niches of Vibrio fischeri in a fully established mutualism. Can J Microbiol 52: 1218-1227.
35. Jones, B.W., Lopez, J.E., Huttenburg, J., and Nishiguchi, M.K. (2006) Population structure between environmentally transmitted vibrios and bobtail squids using nested clade analysis. Mol Ecol 15: 4317-4329.
36. Kierek-Pearson, K., and Karatan, E. (2005) Biofilm development in bacteria. Adv Appl Microbiol 57: 79-111.
37. Kim, Y.R., Lee, S.E., Kim, C.M., Kim, S.Y., Shin, E.K., Shin, D.H., et al. (2003) Characterization and pathogenic significance of Vibrio vulnificus antigens preferentially expressed in septicemic patients. Infect Immun 71: 5461-5471.
38. Lombardo, M.-J., Michalski, J., Martinez-Wilson, H., Morin, C., Hilton, T., Osorio, C.G., et al. (2007) An in vivo expression technology screen for Vibrio cholerae genes expressed in human volunteers. Proc Natl Acad Sci USA 104: 18229-18234.
39. McFall-Ngai, M.J. (1998) The development of cooperative associations between animals and bacteria: establishing détente among domains. Am Zool 38: 593-608.
40. McFall-Ngai, M.J., and Ruby, E.G. (1998) Sepiolids and vibrios: when first they meet. Bioscience 48: 257-265.
41. Mahan, M.J., Heithoff, D.M., Sinsheimer, R.L., and Low, D.A. (2000) Assessment of bacterial pathogenesis by analysis of gene expression in the host. Annu Rev Genet 34: 139-164.
42. Mangan, J.A., Sole, K.M., Mitchison, D.A., and Butcher, P.D. (1997) An effective method of RNA extraction from bacteria refractory to disruption, including mycobacteria. Nucleic Acids Res 25: 675-676.
43. Mekalanos, J.J. (1985) Cholera toxin: genetic analysis, regulation, and the role in pathogenesis. Curr Top Microbiol Immun 118: 97-118.
44. Merrell, D.S., Hava, D.L., and Camilli, A. (2002) Identification of novel factors involved in colonization and acid tolerance of Vibrio cholerae. Mol Microbiol 43: 1471-1491.
45. Moeck, G.S., and Coulton, J.W. (1998) TonB-dependent iron acquisition: mechanisms of siderophore-mediated active transport. Mol Microbiol 28: 675-681.
46. Naidu, A.J., and Yadav, M. (1997) Influence of iron, growth temperature and plasmids on siderophore production in Aeromonas hydrophila. J Med Microbiol 46: 833-838.
47. Nishiguchi, M.K. (2002) Host recognition is responsible for symbiont composition in environmentally transmitted symbiosis. Microbiol Ecol 44: 10-18.
48. Nishiguchi, M.K., Ruby, E.G., and McFall-Ngai, M.J. (1998) Competitive dominance among strains of luminous bacteria provides an unusual form of evidence for parallel evolution in sepiolid squid-Vibrio symbioses. Appl Environ Microbiol 64: 3209-3213.
49. Nootmorn, P., and Chotiyaputta, C. (2002) Species diversity, biomass and community structure of cephalopods off Adang-Rawi Archipelago, Thailand. Bull Mar Sci 71: 591-600.
50. Noriyuki, O., Saito, M., Yamamoto, S., Yoshida, T., Miyoshi, S., and Shinoda, S. (1994) Structure of vulnibactin, a new polyamine-containing siderophore from Vibrio vulnificus. Biometals 7: 109-116.
51. Nyholm, S.V., Stabb, E.V., Ruby, E.G., and McFall-Ngai, M.J. (2000) Establishment of an animal-bacterial association: recruiting symbiotic vibrios from the environment. Proc Natl Acad Sci USA 97: 10231-10235.
52. Owens, L., Austin, D.A., and Austin, B. (1996) Effect of strain origin on siderophore production in Vibrio harveyi isolates. Dis Aquat Organ 27: 157-160.
53. Patel, C.N., Wortham, B.W., Lines, J.L., Fetherston, J.D., Perry, R.D., and Oliveira, M.A. (2006) Polyamines are essential for the formation of plague biofilm. J Bacteriol 188: 2355-2363.
54. Ruby, E.G., and Asato, L.M. (1993) Growth and flagellation of Vibrio fischeri during initiation of the sepiolid squid light organ symbiosis. Arch Microbiol 159: 160-167.
55. Slauch, J.M., Mahan, M.J., and Mekalanos, J.J. (1994) In vivo expression technology for selection of bacterial genes specifically induced in host tissues. Methods Enzymol 235: 481-492.
56. Somboonwiwat, K., Supungul, P., Rimphanitchayakit, V., Aoki, T., Hirono, I., and Tassanakajon, A. (2006) Differentially expressed genes in hemocytes of Vibrio harveyi-challenged shrimp Penaeus monodon. J Biochem Mol Biol 39: 26-36.
57. Soto, W., Gutierrez, J., Remmenga, M.D., and Nishiguchi, M.K. (2009) Salinity and temperature effects on physiological responses of Vibrio fischeri from diverse ecological niches. Microb Ecol 57: 140-150.
58. Stepkowski, T., Brzezinski, K., Legocki, A.B., Jaskólski, M., and Béna, G. (2005) Bayesian phylogenetic analysis reveals two-domain topology of S-adenosylhomocysteine hydrolase protein sequences. Mol Phylogenet Evol 34: 15.
59. Stim, K.P., and Bennett, G.N. (1993) Nucleotide sequence of the adi gene, which encodes the biodegradative acidinduced arginine decarboxylase of Escherichia coli. J Bacteriol 175: 1221-1234.
60. Svitil, A.L., Chadhain, S., Moore, J.A., and Kirchman, D.L. (1997) Chitin degradation proteins produced by the marine bacterium Vibrio harveyi growing on different forms of chitin. Appl Environ Microbiol 63: 408-413.
61. Tarleton, J.C., and Ely, B. (1991) Isolation and characterization of ilvA, ilvBN, and ilvD mutants of Caulobacter crescentus. J Bacteriol 173: 1259-1267.
62. Voet, D., and Voet, J.G. (2004) Biochemistry. Hoboken, NJ, USA: John Wiley & Sons.
63. Wolf, M.K., and Crosa, J.H. (1986) Evidence for the role of a siderophore in promoting Vibrio anguillarum infections. J Gen Microbiol 132: 2944-2952.
64. Yu, C., Lee, A.M., Bassler, B.L., and Roseman, S. (1991) Chitin utilization by marine bacteria. A physiological function for bacterial adhesion to immobilized carbohydrates. J Biol Chem 266: 24260-24267.
65. Zavilgelsky, G.B., Kotova, V.Y., Mazhul, M.M., and Manukhov, I.V. (2004) The effect of Clp proteins on DnaK-dependent refolding of bacterial luciferases. Mol Biol (Moscow) 38: 427-433.