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Genomic polymorphism in symbiotic populations of Photobacterium leiognathi

dc.contributor.authorDunlap, Paul V.en_US
dc.contributor.authorJiemjit, Anchaleeen_US
dc.contributor.authorAst, Jennifer C.en_US
dc.contributor.authorPearce, Meghan M.en_US
dc.contributor.authorMarques, Ryan R.en_US
dc.contributor.authorLavilla-Pitogo, Celia R.en_US
dc.date.accessioned2010-06-01T22:18:24Z
dc.date.available2010-06-01T22:18:24Z
dc.date.issued2004-02en_US
dc.identifier.citationDunlap, Paul V.; Jiemjit, Anchalee; Ast, Jennifer C.; Pearce, Meghan M.; Marques, Ryan R.; Lavilla-Pitogo, Celia R. (2004). "Genomic polymorphism in symbiotic populations of Photobacterium leiognathi ." Environmental Microbiology 6(2): 145-158. <http://hdl.handle.net/2027.42/75318>en_US
dc.identifier.issn1462-2912en_US
dc.identifier.issn1462-2920en_US
dc.identifier.urihttps://hdl.handle.net/2027.42/75318
dc.identifier.urihttp://www.ncbi.nlm.nih.gov/sites/entrez?cmd=retrieve&db=pubmed&list_uids=14756879&dopt=citationen_US
dc.description.abstractPhotobacterium leiognathi forms a bioluminescent symbiosis with leiognathid fishes, colonizing the internal light organ of the fish and providing its host with light used in bioluminescence displays. Strains symbiotic with different species of the fish exhibit substantial phenotypic differences in symbiosis and in culture, including differences in 2-D PAGE protein patterns and profiles of indigenous plasmids. To determine if such differences might reflect a genetically based symbiont-strain/host-species specificity, we profiled the genomes of P. leiognathi strains from leiognathid fishes using PFGE. Individual strains from 10 species of leiognathid fishes exhibited substantial genomic polymorphism, with no obvious similarity among strains; these strains were nonetheless identified as P. leiognathi by 16S rDNA sequence analysis. Profiling of multiple strains from individual host specimens revealed an oligoclonal structure to the symbiont populations; typically one or two genomotypes dominated each population. However, analysis of multiple strains from multiple specimens of the same host species, to determine if the same strain types consistently colonize a host species, demonstrated substantial heterogeneity, with the same genomotype only rarely observed among the symbiont populations of different specimens of the same host species. Colonization of the leiognathid light organ to initiate the symbiosis therefore is likely to be oliogoclonal, and specificity of the P. leiognathi /leiognathid fish symbiosis apparently is maintained at the bacterial species level rather than at the level of individual, genomotypically defined strain types.en_US
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dc.publisherBlackwell Publishing Ltden_US
dc.rights2004 Society for Applied Microbiology and Blackwell Publishing Ltden_US
dc.titleGenomic polymorphism in symbiotic populations of Photobacterium leiognathien_US
dc.typeArticleen_US
dc.subject.hlbsecondlevelMicrobiology and Immunologyen_US
dc.subject.hlbtoplevelScienceen_US
dc.description.peerreviewedPeer Revieweden_US
dc.contributor.affiliationumDepartment of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, USA.en_US
dc.contributor.affiliationotherSidney Kimmel Comprehensive Cancer Center, Johns Hopkins University, Baltimore, MD 21287, USA.en_US
dc.contributor.affiliationotherDepartment of Bacterial Diseases, Walter Reed Army Institute of Research, Silver Spring, MD 20852, USA.en_US
dc.contributor.affiliationotherAquaculture Department, Southeast Asian Fisheries Development Center, Tigbauan 5021, Iloilo, Philippines.en_US
dc.identifier.pmid14756879en_US
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/75318/1/j.1462-2920.2003.00548.x.pdf
dc.identifier.doi10.1046/j.1462-2920.2003.00548.xen_US
dc.identifier.sourceEnvironmental Microbiologyen_US
dc.identifier.citedreferenceAbe, T. ( 1976 ) Keys to the Japanese Fishes, 6th edn. Tokyo, Japan: Hokuryukan.en_US
dc.identifier.citedreferenceAhrens, G. ( 1965 ) Untersuchungen am Leuchtorgan von Leiognathus klunzingeri. Zwiss Zool 0: 90 – 113.en_US
dc.identifier.citedreferenceBassot, J. -M. ( 1975 ) Les organes lumineux a bactÉries symbiotiques de quelques TÉlÉostÉens leiognathides. Arch Zool Exp Gen 116: 359 – 373.en_US
dc.identifier.citedreferenceBoisvert, H., Chatelain, R., and Bassot, J. M. ( 1967 ) Étude d’un Photobacterium isolÉ de l’organe lumineux des poissons Leiognathidae. Ann Inst Pasteur (Paris) 112: 520 – 524.en_US
dc.identifier.citedreferenceBuchrieser, C., Gangar, V. V., Murphee, R. L., Tamplin, M. L., and Kaspar, C. W. ( 1995 ) Multiple Vibrio vulnificus strains in oysters as demonstrated by clamped homogenous electric field gel electrophoresis. Appl Environ Microbiol 61: 1163 – 1168.en_US
dc.identifier.citedreferenceCallahan, S. M., and Dunlap, P. V. ( 2000 ) LuxR- and acyl-homoserine-lactone-controled non- lux genes define a quorum-sensing regulon in Vibrio fischeri. J Bacteriol 182: 2811 – 2822.en_US
dc.identifier.citedreferenceColquhoun, D. J., and Sorum, H. ( 2002 ) Cloning, characterisation and phylogenetic analysis of the fur gene in Vibrio salmonicida and Vibrio logei. Gene 296: 213 – 220.en_US
dc.identifier.citedreferenceDorsch, M., Lane, D., and Stackebrandt, E. ( 1992 ) Towards a phylogeny of the genus Vibrio based on 16S rRNA sequences. Int J Syst Bacteriol 42: 58 – 63.en_US
dc.identifier.citedreferenceDunlap, P. V. ( 1985 ) Physiological and morphological state of the symbiotic bacteria from light organs of ponyfish. Biol Bull 167: 410 – 425.en_US
dc.identifier.citedreferenceDunlap, P. V., and Kita-Tsukamoto, K. ( 2001 ) Luminous bacteria. In The Prokaryotes, an Evolving Electronic Resource for the Microbiological Community. Dworkin, M., Falkow, S., Rosenberg, E. Schleifer, K. -H., Stackebrandt, E., (eds). New York: Academic Press.en_US
dc.identifier.citedreferenceDunlap. P. V., and McFall-Ngai, M. J. ( 1984 ) Leiognathus Elongatus. Perciformes: Leiognathidae): two distinct species based on morphological and light organ characters. Copeia 1984: 884 – 892.en_US
dc.identifier.citedreferenceDunlap. P. V., and McFall-Ngai, M. J. ( 1987 ) Initiation and control of the bioluminescent symbiosis between Photobacterium leiognathi and leiognathid fish. Ann New York Acad Sci 503: 269 – 283.en_US
dc.identifier.citedreferenceDunlap. P. V., and Steinman, H. M. ( 1986 ) Strain variation in bacteriocuprein superoxide dismutase from symbiotic Photobacterium leiognathi. J Bacteriol 165: 393 – 398.en_US
dc.identifier.citedreferenceFischer-Le Saux, M., Viallard, V., Brunel, B., Normand, P., and Boemare, N. E. ( 1999 ). Polyphasic classification of the genus Photorhabdus, proposal of new taxa: P. luminescens subsp. luminescens subsp. nov, P. luminescens subsp. akhurstii subsp. nov., P. luminescens subsp. laumondii subsp. nov., P. temperata sp. nov., P. temperata subsp temperata subsp. nov., P. asymbiotica sp. nov. Int J and Syst Bacteriol 49: 1645 – 1656en_US
dc.identifier.citedreferenceFroese, R., and Pauly, D., eds. ( 2003 ) FishBase. [WWW document]. URL http://www.fishbase.org.en_US
dc.identifier.citedreferenceGauthier, G., Gauthier, M., and Christen, R. ( 1995 ) Phylogenetic analysis of the genera Alteromonas, Shewanella, and Moritella using genes coding for small-subunit rRNA sequences and division of the genus Alteromonas into two genera Alteromonas (emended) and Pseudoalteromonas gen. nov. and proposal of twelve new species combinations. Int J Syst Bact 45: 755 – 761.en_US
dc.identifier.citedreferenceGÜrtler, V., and Mayall, B. C. ( 2001 ) Genomic approaches to typing, taxonomy and evolution of bacterial isolates. Int J Syst Evol Microbiol 51: 3 – 16.en_US
dc.identifier.citedreferenceHaneda, Y. ( 1940 ) On the luminescence of fishes belonging to the family Leiognathidae of the tropical Pacific. Palao Trop Biol Stn Stud 2: 29 – 39.en_US
dc.identifier.citedreferenceHaneda, Y. ( 1950 ) Luminous organs of fish that emit light indirectly. Pacif Sci 4: 214 – 277.en_US
dc.identifier.citedreferenceHaneda, Y., and Tsuji, F. I. ( 1976 ) The luminescent systems of pony fishes. J Morphol 150: 539 – 552.en_US
dc.identifier.citedreferenceHarms, J. W. ( 1928 ) Bau und Entwicklung eines eigenartigen Leuchtorgans bei Equula spec. Zwiss Zool 131: 157 – 179.en_US
dc.identifier.citedreferenceHastings, J. W. ( 1971 ) Light to hide by: ventral luminescence to camouflage the silhouette. Science 173: 1016 – 1017.en_US
dc.identifier.citedreferenceHastings, J. W., and Mitchell, G. ( 1971 ) Endosymbiotic bioluminescent bacteria from the light organs of pony fish. Biol Bull Mar Biol Laboratory Woods Hole 141: 261 – 268.en_US
dc.identifier.citedreferenceHerring, P. J., and Morin, J. G. ( 1978 ) Bioluminescence in fishes. In Bioluminescence In Action. Herring, P. J., (ed.). London: Academic Press, pp. 273 – 329.en_US
dc.identifier.citedreferenceKimura, S., Yamashita, T., and Iwatsuki, Y. ( 2000 ) A new species, Gazza rhombea, from the Indo-West Pacific, with a redescription of G. achlamys Jordan & Starks 1917 (Perciformes: Leiognathidae). Ichthyol Res 47: 1 – 12.en_US
dc.identifier.citedreferenceKimura, S., Dunlap, P. V., Peristiwady, T., and Lavilla-Pitogo, C. R. ( 2003 ) The Leiognathus aureus complex (Perciformes: Leiognathidae) with the description of a new species. Ichthyol Res 50: 221 – 232.en_US
dc.identifier.citedreferenceKita-Tsukamoto, K., Oyaizu, H., Nanba, K., and Simidu, U. ( 1993 ) Phylogenetic relationships of marine bacteria, mainly members of the family Vibrionaceae, determined on the basis of 16S rRNA sequences. Int J Syst Bacteriol 43: 8 – 19.en_US
dc.identifier.citedreferenceLane, D. J. ( 1991 ) 16S/23S rRNA sequencing. In Nucleic Acid Techniques in Bacterial Systematics. Stackebrandt, E. and Goodfellow, M., (eds). Chichester, NY: J. Wiley and Sons, pp. 115 – 175.en_US
dc.identifier.citedreferenceLiebana, E., Garcia-Migura, L., Clouting, C., Cassar, C. A., Clifton-Hadley, F. A., Lindsay,. E. A., et al. ( 2002 ) Investigation of the genetic diversity among isolates of Salmonella enterica serovar Dublin from animals and humans from England, Wales and Ireland. J Appl Microbiol 93: 732 – 744.en_US
dc.identifier.citedreferenceMacDonnell, M. T., and Colwell, R. R. ( 1984 ) Nucleotide base sequence of Vibrionaceae 5S rRNA. FEBS Lett 175: 183 – 188.en_US
dc.identifier.citedreferenceMakemson, J. C., Fulayfil, N. R., Landry, W., Van Ert, L. M., Wimpee, C. F., Widder, E. A., and Case, J. F. ( 1997 ) Shewanella woodyi sp. nov., an exclusively respiratory luminous bacterium isolated from the Alboran Sea. Int J Syst Bacteriol 47: 1034 – 1039.en_US
dc.identifier.citedreferenceMcFall-Ngai, M. J. ( 1983a ) The gas bladder as a central component of the leiognathid bacterial light organ symbiosis. Am Zool 23: 907.en_US
dc.identifier.citedreferenceMcFall-Ngai, M. J. ( 1983b ) Adaptation for reflection of bioluminescent light in the gas bladder of Leiognathus equulus (Perciformes: Leiognathidae). J Exp Zool 227: 23 – 33.en_US
dc.identifier.citedreferenceMcFall-Ngai, M. J., and Dunlap, P. V. ( 1983 ) Three new modes of luminescence in the leiognathid fish Gazza minuta: discrete projected luminescence, ventral body flash and buccal luminescence. Mar Biol 73: 227 – 237.en_US
dc.identifier.citedreferenceMcFall-Ngai, M. J., and Dunlap, P. V. ( 1984 ) External and internal sexual dimorphism in leiognathid fishes: morphological evidence for sex-specific bioluminescent signaling. J Morph 182: 71 – 83.en_US
dc.identifier.citedreferenceMcFall-Ngai, M. J., and Morin, J. G. ( 1991 ) Camouflage by disruptive illumination in leiognathids, a family of shallow-water bioluminescent fishes. J Exp Biol 156: 119 – 137.en_US
dc.identifier.citedreferenceMochizuki, K., and Hayashi, M. ( 1989 ) Revision of the leiognathid fishes of the genus Secutor, with two new species. Sci Rep Yokosuka City Mus 37: 83 – 95.en_US
dc.identifier.citedreferenceMonkolprasit, S. ( 1973 ) The fishes of the leiognathid genus Secutor, with the description of a new species from Thailand. Kasetsart Univ Fish Res Bull 6: 10 – 17.en_US
dc.identifier.citedreferenceMorton, A. C., Begg, A. P., Anderson, G. A., Takai, S., Lammler, C., and Browning, G. F. ( 2001 ) Epidemiology of Rhodococcus equi strains on thoroughbred horse farms. Appl Environ Microbiol 67: 2167 – 2175.en_US
dc.identifier.citedreferenceNishiguchi, 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.en_US
dc.identifier.citedreferenceO'Farrell, P. H. ( 1975 ) High-resolution two-dimensional electrophoresis of proteins. J Biol Chem 250: 4007 – 4021.en_US
dc.identifier.citedreferenceOlive, D. M., and Bean, P. ( 1999 ) Principles and applications of methods for DNA-based typing of microbial organisms. J Clin Microbiol 37: 1661 – 1669.en_US
dc.identifier.citedreferenceReichelt, J. L., and Baumann, P. ( 1973 ) Taxonomy of the marine, luminous bacteria. Arch Mikrobiol 94: 283 – 330.en_US
dc.identifier.citedreferenceReichelt, J. L., Nealson, K., and Hastings, J. W. ( 1977 ) The specificity of symbiosis: pony fish and luminescent bacteria. Arch Microbiol 112: 157 – 161.en_US
dc.identifier.citedreferenceRuby, E. G., and Morin, J. G. ( 1978 ) Specificity of symbiosis between deep-sea fish and psychrotrophic luminous bacteria. Deep-Sea Res 25: 161 – 171.en_US
dc.identifier.citedreferenceRuby, E. G., and Nealson, K. H. ( 1976 ) Symbiotic association of Photobacterium fischeri with the marine luminous fish Monocentris japonica: a model of symbiosis based on bacterial studies. Biol Bull 151: 574 – 586.en_US
dc.identifier.citedreferenceRuby, E. G., and Nealson, K. H. ( 1978 ) Seasonal changes in the species composition of luminous bacteria in nearshore seawater. Limnol Oceanogr 23: 530 – 533.en_US
dc.identifier.citedreferenceRuby, E. G., Greenberg, E. P., and Hastings, J. W. ( 1980 ) Planktonic marine luminous bacteria: species distribution in the water column. Appl Environ Microbiol 39: 302 – 306.en_US
dc.identifier.citedreferenceRuimy, R., Breittmayer, V., Elbaze, P., Lafay, B., Boussemart, O., Gauthier, M., and Christen, R. ( 1994 ) Phylogenetic analysis and assessment of the Genera Vibrio, Photobacterium, Aeromonas, and Pleisomonas deduced from small-subunit rRNA sequences. Int J System Bacteriol 44: 416 – 426.en_US
dc.identifier.citedreferenceSingh, D. V., MattÉ, M. H., MattÉ, G. R., Jiang, S., Sabeena, F., Shukla, B. N., et al. ( 2001 ) Molecular analysis of Vibrio cholerae O1, O139, non-O1, and non-O139 strains: clonal relationships between clinical and environmental isolates. Appl Environ Microbiol 67: 910 – 921.en_US
dc.identifier.citedreferenceSorenson, M. D. ( 1999 ) TreeRot, version 2. Boston, MA: Boston University.en_US
dc.identifier.citedreferenceSuwanto, A., Yuhana, M., Herawaty, E., and Angka, S. L. ( 1998 ) Genetic diversity of luminous Vibrio isolated from shrimp larvae. In Advances in Shrimp Biotechnology. Flegel, T. W., (ed.). Bangkok: National Center for Genetic Engineering and Biotechnology, pp. 217 – 224.en_US
dc.identifier.citedreferenceSuzuki, T., Yabusaki, H., and Nishimura, Y. ( 1996 ) Phylogenetic relationships of entomopathogenic nematophilic bacteria: Xenorhabdus spp. & Photorhabdus sp. J Basic Microbiol 36: 351 – 354.en_US
dc.identifier.citedreferenceSwofford, D. L. ( 2002 ) paup*: Phylogenetic analysis using parsimony (*and other methods), Version 4. Sunderland, MA: Sinauer Associates.en_US
dc.identifier.citedreferenceWada, M., Azuma, N., Mizuno, N., and Kurokura, H. ( 1999 ) Transfer of symbiotic luminous bacteria from parental Leiognathus nuchalis to offspring. Mar Biol 135: 683 – 687.en_US
dc.identifier.citedreferenceWallace, R. J. Jr, Zhang, Y., Wilson, R. W., Mann, L., and Rossmoore, H. ( 2002 ) Presence of a single genomotype of the newly described species Mycobacterium immunogenum. industrial metalworking fluids associated with hypersensitivity pneumonitis. Appl Environ Microbiol 68: 5580 – 5584.en_US
dc.identifier.citedreferenceWiik, R., Stackebrandt, E., Valle, O., Daae, F. L., Rodseth, O. M., and Andersen, K. ( 1995 ) Classification of fish-pathogenic vibrios based on comparative 16S rRNA analysis. Int J Syst Bacteriol 45: 421 – 428.en_US
dc.identifier.citedreferenceWolfe, C. J., and Haygood, M. G. ( 1991 ) Restriction fragment length polymorphism analysis reveals high levels of genetic divergence among the light organ symbionts of flashlight fish. Biol Bull 181: 135 – 143.en_US
dc.identifier.citedreferenceWoodland, D. J., Cabanban, A. S., Taylor, V. M., and Taylor, R. J. ( 2002 ) A synchronized rhythmic flashing light display by schooling Leiognathus splendens (Leiognathidae: Perciformes). Mar Freshwater Res 53: 159 – 162.en_US
dc.identifier.citedreferenceWoodland, D. J., Premchaoen, S., and Cabanban, A. S. ( 2001 ) Leiognathidae. In FAO Species Identification Guide for Fishery Purposes. The Living Marine Resources of the Western Central Pacific, vol. 5 Bony Fishes Part 3 (Menidae to Pomacentridae). Carpenter, K. E., and Niem, V. H., (eds). Rome: FAO, pp. 2792 – 2823.en_US
dc.identifier.citedreferenceYamashita, T., and Kimura, S., and Iwatsuki, Y. ( 1998 ) Validity of the leiognathid fish, Gazza dentex (Valenciennes in Cuvier and Valenciennes, 1835), with designation of a lectotype and redescription of G. minuta (Bloch, 1795). Ichthyol Res 45: 271 – 280.en_US
dc.identifier.citedreferenceYetinson, T., and Shilo, M. ( 1979 ) Seasonal and geographic distribution of luminous bacteria in the. Eastern Mediterranean Sea and the Gulf of Elat. Appl Environ Microbiol 37: 1230 – 1238.en_US
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