Marine Biotechnology

, Volume 17, Issue 4, pp 463–478 | Cite as

The Pathogen of the Great Barrier Reef Sponge Rhopaloeides odorabile Is a New Strain of Pseudoalteromonas agarivorans Containing Abundant and Diverse Virulence-Related Genes

  • Jayanta D. Choudhury
  • Arnab Pramanik
  • Nicole S. Webster
  • Lyndon E. Llewellyn
  • Ratan Gachhui
  • Joydeep MukherjeeEmail author
Original Article


Sponge diseases have increased dramatically, yet the causative agents of disease outbreaks have eluded identification. We undertook a polyphasic taxonomic analysis of the only confirmed sponge pathogen and identified it as a novel strain of Pseudoalteromonas agarivorans. 16S ribosomal RNA (rRNA) and gyraseB (gyrB) gene sequences along with phenotypic characteristics demonstrated that strain NW4327 was most closely related to P. agarivorans. DNA-DNA hybridization and in silico genome comparisons established NW4327 as a novel strain of P. agarivorans. Genes associated with type IV pili, mannose-sensitive hemagglutinin pili, and curli formation were identified in NW4327. One gene cluster encoding ATP-binding cassette (ABC) transporter, HlyD and TolC, and two clusters related to the general secretion pathway indicated the presence of type I secretion system (T1SS) and type II secretion system (T2SS), respectively. A contiguous gene cluster of at least 19 genes related to type VI secretion system (T6SS) which included all 13 core genes was found. The absence of T1SS and T6SS in nonpathogenic P. agarivorans S816 established NW4327 as the virulent strain. Serine proteases and metalloproteases of the classes S8, S9, M4, M6, M48, and U32 were identified in NW4327, many of which can degrade collagen. Collagenase activity in NW4327 and its absence in the nonpathogenic P. agarivorans KMM 255T reinforced the invasiveness of NW4327. This is the first report unambiguously identifying a sponge pathogen and providing the first insights into the virulence genes present in any pathogenic Pseudoalteromonas genome. The investigation supports a theoretical study predicting high abundance of terrestrial virulence gene homologues in marine bacteria.


Pseudoalteromonas Sponge disease Taxonomy Genome analysis Collagenase 



Financial support through sanction no. SR/SO/BB-0114/2010 to JM and RG and INSPIRE fellowship no. IF110045 to JDC from the Department of Science and Technology (, Ministry of Science and Technology, Government of India is thankfully acknowledged. NSW was funded through an Australian Research Council Future Fellowship (FT120100480).

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

10126_2015_9627_MOESM1_ESM.doc (552 kb)
ESM 1 (DOC 552 kb)


  1. Akagawa M, Yamasato K (1989) Synonymy of Alcaligenes aquamarinus, Alcaligenes faecalis subsp. homari, and Deleya aesta: Deleya aquamarina comb. nov. as the type species of the genus Deleya. Int J Syst Bacteriol 39:462–466CrossRefGoogle Scholar
  2. Angermeier H, Kamke J, Abdelmohsen UR, Krohne G, Pawlik JR, Lindquist NL, Hentschel U (2011) The pathology of sponge orange band disease affecting the Caribbean barrel sponge Xestospongia muta. FEMS Microbiol Ecol 75:218–230PubMedCrossRefGoogle Scholar
  3. Angermeier H, Glöckner V, Pawlik JR, Lindquist NL, Hentschel U (2012) Sponge white patch disease affecting the Caribbean sponge Amphimedon compressa. Dis Aquat Org 99:95–102PubMedCrossRefGoogle Scholar
  4. Arumugam M, Mitra A, Pramanik A, Saha M, Gachhui R, Mukherjee J (2011) Streptomyces sundarbansensis sp. nov., an actinomycete that produces 2-allyloxyphenol. Int J Syst Evol Microbiol 61:2664–2669PubMedCrossRefGoogle Scholar
  5. Auch AF, von Jan M, Klenk H-P, Göker M (2010) Digital DNA-DNA hybridization for microbial species delineation by means of genome-to-genome sequence comparison. Stand Genomic Sci 2:117–134. doi: 10.4056/sigs.531120 PubMedCentralPubMedCrossRefGoogle Scholar
  6. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O (2008) The RAST server: rapid annotations using subsystems technology. BMC Genomics 9:75. doi: 10.1186/1471-2164-9-75 PubMedCentralPubMedCrossRefGoogle Scholar
  7. Barrow G, Feltham RKA (1993) Cowan and Steel’s manual for the identification of medical bacteria, 3rd edn. Cambridge University Press, New YorkCrossRefGoogle Scholar
  8. Barry AI (1980) Procedures and theoretical considerations for testing antimicrobial agents in agar media. In: Logan V (ed) Antibiotics in laboratory medicine. William & Wilkins, Baltimore, pp 10–16Google Scholar
  9. Baumann P, Baumann L (1981) The marine Gram-negative eubacteria; genera Photobacterium, Beneckea, Alteromonas, Pseudomonas, and Alcaligenes. In: Starr P, Stolp H, Triiper HG, Balows A, Schlegel HG (eds) The prokaryotes: a handbook on habitats, isolation, and identification of bacteria, vol 2, 1st edn. Springer, Berlin, pp 1302–1330Google Scholar
  10. Baumann P, Baumann L, Mandel M (1971) Taxonomy of marine bacteria: the genus Beneckea. J Bacteriol 107:268–294PubMedCentralPubMedGoogle Scholar
  11. Baumann L, Baumann P, Mandel M, Allen RD (1972) Taxonomy of aerobic marine eubacteria. J Bacteriol 110:402–429PubMedCentralPubMedGoogle Scholar
  12. Bendtsen JD, Kiemer L, Fausbøll A, Brunak S (2005) Non-classical protein secretion in bacteria. BMC Microbiol 5:58. doi: 10.1186/1471-2180-5-58 PubMedCentralPubMedCrossRefGoogle Scholar
  13. Bingle LE, Bailey CM, Pallen MJ (2008) Type VI secretion: a beginner’s guide. Curr Opin Microbiol 11:3–8PubMedCrossRefGoogle Scholar
  14. Bjornsdottir B, Fridjonsson OH, Magnusdottir S, Andresdottir V, Hreggvidsson GO, Gudmundsdottir BK (2009) Characterisation of an extracellular vibriolysin of the fish pathogen Moritella viscosa. Vet Microbiol 136:326–334PubMedCrossRefGoogle Scholar
  15. Bladergroen MR, Badelt K, Spaink HP (2003) Infection-blocking genes of a symbiotic Rhizobium leguminosarum strain that are involved in temperature-dependent protein secretion. Mol Plant Microbe Interact 16:53–64PubMedCrossRefGoogle Scholar
  16. Boyer F, Fichant G, Berthod J, Vandenbrouck Y, Attree I (2009) Dissecting the bacterial type VI secretion system by a genome wide in silico analysis: what can be learned from available microbial genomic resources? BMC Genomics 10:104. doi: 10.1186/1471-2164-10-104 PubMedCentralPubMedCrossRefGoogle Scholar
  17. Burdon KL (1946) Fatty materials in bacteria and fungi revealed by staining dried, fixed slide preparations. J Bacteriol 52:665–678PubMedCentralPubMedGoogle Scholar
  18. Cervino JM, Winiarski-Cervino K, Polson SW, Goreau T, Smith GW (2006) Identification of bacteria associated with a disease affecting the marine sponge Ianthella basta in New Britain, Papua New Guinea. Mar Ecol Prog Ser 324:139–150CrossRefGoogle Scholar
  19. Choudhury JD, Pramanik A, Webster NS, Llewellyn LE, Gachhui R, Mukherjee J (2014) Draft genome sequence of Pseudoalteromonas sp. strain NW 4327 (MTCC 11073, DSM 25418), a pathogen of the Great Barrier Reef sponge Rhopaloeides odorabile. Genome Announc 2:e00001–e00014. doi: 10.1128/genomeA. 00001-14 PubMedCentralPubMedCrossRefGoogle Scholar
  20. Coulthurst SJ (2013) The type VI secretion system—a widespread and versatile cell targeting system. Res Microbiol 164:640–654PubMedCrossRefGoogle Scholar
  21. Dalisay DS, Webb JS, Scheffel A, Svenson C, James S, Holmström C, Egan S, Kjelleberg S (2006) A mannose-sensitive haemagglutinin (MSHA)-like pilus promotes attachment of Pseudoalteromonas tunicata cells to the surface of the green alga Ulva australis. Microbiology 152:2875–2883PubMedCrossRefGoogle Scholar
  22. Darling ACE, Mau B, Blattner FR, Perna NT (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14:1394–1403PubMedCentralPubMedCrossRefGoogle Scholar
  23. de O Santos E, Alves N Jr, Dias GM, Mazotto AM, Vermelho A, Vora GJ, Wilson B, Beltran VH, Bourne DG, Le Roux F, Thompson FL (2011) Genomic and proteomic analyses of the coral pathogen Vibrio coralliilyticus reveal a diverse virulence repertoire. ISME J 5:1471–1483Google Scholar
  24. Delepelaire P (2004) Type I secretion in gram-negative bacteria. Biochim Biophys Acta 1694:279–297CrossRefGoogle Scholar
  25. Dueholm MS, Albertsen M, Otzen D, Nielsen PH (2012) Curli functional amyloid systems are phylogenetically widespread and display large diversity in operon and protein structure. PLoS One 7:e51274. doi: 10.1371/journal.pone.0051274 PubMedCentralPubMedCrossRefGoogle Scholar
  26. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM (2007) DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57:81–91PubMedCrossRefGoogle Scholar
  27. Hallin PF, Stærfeldt H-H, Rotenberg E, Binnewies TT, Benham CJ, Ussery DW (2009) GeneWiz browser: an interactive tool for visualizing sequenced chromosomes. Stand Genomic Sci 1:204–215. doi: 10.4056/sigs.28177 PubMedCentralPubMedCrossRefGoogle Scholar
  28. Hiraishi A, Shin YK, Sugiyama J (1992) Rapid profiling of bacterial quinones by two-dimensional thin-layer chromatography. Lett Appl Microbiol 14:170–173CrossRefGoogle Scholar
  29. Hoge R, Pelzer A, Rosenau F, Wilhelm S (2010) Weapons of a pathogen: proteases and their role in virulence of Pseudomonas aeruginosa. In: Mendez-Vilas A (ed) Microbiology book series—current research, technology and education topics in applied microbiology and microbial biotechnology, number 2. Formatex Research Center, Spain, pp 383–395Google Scholar
  30. Ivanova EP, Kiprianova EA, Mikhailov VV, Levanova GF, Garagulya AD, Gorshkova NM, Yumoto N, Yoshikawa S (1996) Characterization and identification of marine Alteromonas nigrifaciens strains and emendation of the description. Int J Syst Bacteriol 46:223–228CrossRefGoogle Scholar
  31. Ivanova EP, Zhukova NV, Svetashev VI, Gorshkova NM, Kurilenko VV, Frolova GM, Mikhailov VV (2000) Evaluation of phospholipid and fatty acid compositions as chemotaxonomic markers of Alteromonas-like proteobacteria. Curr Microbiol 41:341–345PubMedCrossRefGoogle Scholar
  32. Ivanova EP, Bakunina IY, Nedashkovskaya OI, Gorshkova NM, Alexeeva YV, Zelepuga EA, Zvaygintseva TN, Nicolau DV, Mikhailov VV (2003) Ecophysiological variabilities in ectohydrolytic enzyme activities of some Pseudoalteromonas species, P. citrea, P. issachenkonii, and P. nigrifaciens. Curr Microbiol 46:6–10PubMedCrossRefGoogle Scholar
  33. Jakobsen TH, Hansen MA, Jensen PØ, Hansen L, Riber L, Cockburn A, Kolpen M, Hansen CR, Ridderberg W, Eickhardt S, Hansen M, Kerpedjiev P, Alhede M, Qvortrup K, Burmølle M, Moser C, Kühl M, Ciofu O, Givskov M, Sørensen SJ, Høiby N, Bjarnsholt T (2013) Complete genome sequence of the cystic fibrosis pathogen Achromobacter xylosoxidans NH44784-1996 complies with important pathogenic phenotypes. PLoS One 8:e68484. doi: 10.1371/journal.pone.0068484 PubMedCentralPubMedCrossRefGoogle Scholar
  34. Kavermann H, Burns BP, Angermüller K, Odenbreit S, Fischer W, Melchers K, Haas R (2003) Identification and characterization of Helicobacter pylori genes essential for gastric colonization. J Exp Med 197:813–822PubMedCentralPubMedCrossRefGoogle Scholar
  35. Kim O-S, Cho Y-J, Lee K, Yoon S-H, Kim M, Na H, Park S-C, Jeon YS, Lee J-H, Yi H, Won S, Chun J (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721PubMedCrossRefGoogle Scholar
  36. Kimes NE, Grim CJ, Johnson WR, Hasan NA, Tall BD, Kothary MH, Kiss H, Munk AC, Tapia R, Green L, Detter C, Bruce DC, Brettin TS, Colwell RR, Morris PJ (2012) Temperature regulation of virulence factors in the pathogen Vibrio coralliilyticus. ISME J 6:835–846PubMedCentralPubMedCrossRefGoogle Scholar
  37. Kuykendall LD, Roy MA, O’Neill JJ, Devine TE (1988) Fatty acids, antibiotic resistance, and deoxyribonucleic acid homology groups of Bradyrhizobium japonicum. Int J Syst Bacteriol 38:358–361CrossRefGoogle Scholar
  38. Liu H, Zheng F, Sun X, Hong X, Dong S, Wang B, Tang X, Wang Y (2010) Identification of the pathogens associated with skin ulceration and peristome tumescence in cultured sea cucumbers Apostichopus japonicus (Selenka). J Invertebr Pathol 105:236–242PubMedCrossRefGoogle Scholar
  39. Luter HM, Whalan S, Webster NS (2010a) Prevalence of tissue necrosis and brown spot lesions in a common marine sponge. Mar Freshw Res 61:484–489CrossRefGoogle Scholar
  40. Luter HM, Whalan S, Webster NS (2010b) Exploring the role of microorganisms in the disease-like syndrome affecting the sponge Ianthella basta. Appl Environ Microbiol 76:5736–5744PubMedCentralPubMedCrossRefGoogle Scholar
  41. Maldonado M, Sánchez-Tocino L, Navarro C (2010) Recurrent disease outbreaks in corneous demosponges of the genus Ircinia: epidemic incidence and defense mechanisms. Mar Biol 157:1577–1590CrossRefGoogle Scholar
  42. Marmur J, Doty P (1962) Determination of the base composition of deoxyribonucleic acid from its thermal denaturation temperature. J Mol Biol 5:109–118PubMedCrossRefGoogle Scholar
  43. Meier-Kolthoff JP, Göker M, Spröer C, Klenk H-P (2013) When should a DDH experiment be mandatory in microbial taxonomy? Arch Microbiol 195:413–418PubMedCrossRefGoogle Scholar
  44. Mikhailov VV, Romanenko LA, Ivanova EP (2002) The genus Alteromonas and related Proteobacteria. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes vol 6, release 3.10, 3rd edn. Springer, New YorkGoogle Scholar
  45. Miller LT (1982) Single derivatization method for routine analysis of bacterial whole-cell fatty acid methyl esters, including hydroxy acids. J Clin Microbiol 16:584–586PubMedCentralPubMedGoogle Scholar
  46. Mougous JD, Gifford CA, Ramsdell TL, Mekalanos JJ (2007) Threonine phosphorylation post-translationally regulates protein secretion in Pseudomonas aeruginosa. Nat Cell Biol 9:797–803PubMedCrossRefGoogle Scholar
  47. Mukherjee J, Webster N, Llewellyn LE (2009) Purification and characterization of a collagenolytic enzyme from a pathogen of the Great Barrier Reef sponge, Rhopaloeides odorabile. PLoS One 4:e7177. doi: 10.1371/journal.pone.0007177 PubMedCentralPubMedCrossRefGoogle Scholar
  48. Nelson EJ, Ghiorse WC (1999) Isolation and identification of Pseudoalteromonas piscicida strain Cura-d associated with diseased damselfish (Pomacentridae) eggs. J Fish Dis 22:253–260CrossRefGoogle Scholar
  49. Nieto C, Cherny I, Khoo SK, de Lacoba MG, Chan WT, Yeo CC, Gazit E, Espinosa M (2007) The yefM-yoeB toxin-antitoxin systems of Escherichia coli and Streptococcus pneumoniae: functional and structural correlation. J Bacteriol 189:1266–1278PubMedCentralPubMedCrossRefGoogle Scholar
  50. Oh Y-S, Park A-R, Lee J-K, Lim C-S, Yoo J-S, Roh D-H (2011) Pseudoalteromonas donghaensis sp. nov., isolated from seawater. Int J Syst Evol Microbiol 61:351–355PubMedCrossRefGoogle Scholar
  51. Olson JB, Thacker RW, Gochfeld DJ (2014) Molecular community profiling reveals impacts of time, space, and disease status on the bacterial community associated with the Caribbean sponge Aplysina cauliformis. FEMS Microbiol Ecol 87:268–279PubMedCrossRefGoogle Scholar
  52. Park JR, Bae J-W, Nam Y-D, Chang H-W, Kwon H-Y, Quan Z-X, Park Y-H (2007) Sulfitobacter litoralis sp. nov., a marine bacterium isolated from the East Sea, Korea. Int J Syst Evol Microbiol 57:692–695PubMedCrossRefGoogle Scholar
  53. Parrilli E, Giuliani M, Tutino ML (2008) General secretory pathway from marine Antarctic Pseudoalteromonas haloplanktis TAC125. Mar Genomics 1:123–128PubMedCrossRefGoogle Scholar
  54. Persson OP, Pinhassi J, Riemann L, Marklund B-I, Rhen M, Normark S, González JM, Hagström Å (2009) High abundance of virulence gene homologues in marine bacteria. Environ Microbiol 11:1348–1357PubMedCentralPubMedCrossRefGoogle Scholar
  55. Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785–786PubMedCrossRefGoogle Scholar
  56. Pukatzki S, Ma AT, Sturtevant D, Krastins B, Sarracino D, Nelson WC, Heidelberg JF, Mekalanos JJ (2006) Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc Natl Acad Sci U S A 103:1528–1533PubMedCentralPubMedCrossRefGoogle Scholar
  57. Rainey FA, Ward-Rainey N, Kroppenstedt RM, Stackebrandt E (1996) The genus Nocardiopsis represents a phylogenetically coherent taxon and a distinct actinomycete lineage: proposal of Nocardiopsaceae fam. nov. Int J Syst Bacteriol 46:1088–1092PubMedCrossRefGoogle Scholar
  58. Reshef L, Ron E, Rosenberg E (2008) Genome analysis of the coral bleaching pathogen Vibrio shiloi. Arch Microbiol 190:185–194PubMedCrossRefGoogle Scholar
  59. Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A 106:19126–19131PubMedCentralPubMedCrossRefGoogle Scholar
  60. Ridgway ID, Small HJ, Atkinson RJA, Birkbeck HT, Taylor AC, Neil DM (2008) Extracellular proteases and possible disease related virulence mechanisms of two marine bacteria implicated in an opportunistic bacterial infection of Nephrops norvegicus. J Invertebr Pathol 99:14–19PubMedCrossRefGoogle Scholar
  61. Romanenko LA, Zhukova NV, Rohde M, Lysenko AM, Mikhailov VV, Stackebrandt E (2003) Pseudoalteromonas agarivorans sp. nov., a novel marine agarolytic bacterium. Int J Syst Evol Microbiol 53:125–131PubMedCrossRefGoogle Scholar
  62. Sawabe T, Tanaka R, Iqbal MM, Tajima K, Ezura Y, Ivanova EP, Christen R (2000) Assignment of Alteromonas elyakovii KMM 162T and five strains isolated from spot-wounded fronds of Laminaria japonica to Pseudoalteromonas elyakovii comb. nov. and the extended description of the species. Int J Syst Evol Microbiol 50:265–271PubMedCrossRefGoogle Scholar
  63. Smibert RM, Krieg NR (1993) Phenotypic characterization. In: Gerhardt P, Murray RGE, Wood WA, Krieg NR (eds) Methods for general and molecular bacteriology. American Society for Microbiology, Washington, pp 607–654Google Scholar
  64. Song JK, Kim D, Eun J-B, Choi B-D, Oh MJ, Jung SJ (2012) Identification of cellulolytic bacteria associated with tunic softness syndrome in the sea squirt, Halocynthia roretzi. Food Sci Biotechnol 21:1405–1411CrossRefGoogle Scholar
  65. Sorokin DY (1995) Sulfitobacter pontiacus gen. nov., sp. nov.—a new heterotrophic bacterium from the Black Sea, specialized on sulfite oxidation. Microbiology 64:354–365Google Scholar
  66. Stabili L, Cardone F, Alifano P, Tredici SM, Piraino S, Corriero G, Gaino E (2012) Epidemic mortality of the sponge Ircinia variabilis (Schmidt, 1862) associated to proliferation of a Vibrio bacterium. Microb Ecol 64:802–813PubMedCrossRefGoogle Scholar
  67. Stackebrandt E, Ebers J (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 33:152–155Google Scholar
  68. Teeling H, Meyerdierks A, Bauer M, Amann R, Glöckner FO (2004) Application of tetranucleotide frequencies for the assignment of genomic fragments. Environ Microbiol 6:938–947PubMedCrossRefGoogle Scholar
  69. Thomas T, Evans FF, Schleheck D, Mai-Prochnow A, Burke C, Penesyan A, Dalisay DS, Stelzer-Braid S, Saunders N, Johnson J, Ferriera S, Kjelleberg S, Egan S (2008) Analysis of the Pseudoalteromonas tunicata genome reveals properties of a surface-associated life style in the marine environment. PLoS One 3:e3252. doi: 10.1371/journal.pone.0003252 PubMedCentralPubMedCrossRefGoogle Scholar
  70. Tindall BJ, Rosselló-Móra R, Busse H-J, Ludwig W, Kämpfer P (2010) Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol 60:249–266PubMedCrossRefGoogle Scholar
  71. Van Sluys MA, Monteiro-Vitorello CB, Camargo LEA, Menck CFM, da Silva ACR, Ferro JA, Oliveira MC, Setubal JC, Kitajima JP, Simpson AJ (2002) Comparative genomic analysis of plant-associated bacteria. Annu Rev Phytopathol 40:169–189PubMedCrossRefGoogle Scholar
  72. Venkateswaran K, Dohmoto N (2000) Pseudoalteromonas peptidolytica sp. nov., a novel marine mussel-thread-degrading bacterium isolated from the Sea of Japan. Int J Syst Evol Microbiol 50:565–574PubMedCrossRefGoogle Scholar
  73. Venkateswaran K, Moser DP, Dollhopf ME, Lies DP, Saffarini DA, MacGregor BJ, Ringelberg DB, White DC, Nishijima M, Sano H, Burghardt J, Stackebrandt E, Nealson KH (1999) Polyphasic taxonomy of the genus Shewanella and description of Shewanella oneidensis sp. nov. Int J Syst Bacteriol 49:705–724PubMedCrossRefGoogle Scholar
  74. Vynne NG, Månsson M, Nielsen KF, Gram L (2011) Bioactivity, chemical profiling, and 16S rRNA-based phylogeny of Pseudoalteromonas strains collected on a global research cruise. Mar Biotechnol 13:1062–1073PubMedCrossRefGoogle Scholar
  75. Wang Y, Feng N, Li Q, Ding J, Zhan Y, Chang Y (2013) Isolation and characterization of bacteria associated with a syndrome disease of sea urchin Strongylocentrotus intermedius in North China. Aquacult Res 44:691–700CrossRefGoogle Scholar
  76. Wayne LG, Brenner DJ, Colwell RR, Grimont PAD, Kandler O, Krichevsky MI, Moore LH, Moore WEC, Murray RGE, Stackebrandt E, Starr MP, Truper HG (1987) Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int J Syst Bacteriol 37:463–464CrossRefGoogle Scholar
  77. Webster NS (2007) Sponge disease: a global threat? Environ Microbiol 9:1363–1375PubMedCrossRefGoogle Scholar
  78. Webster NS, Negri AP, Webb RI, Hill RT (2002) A spongin-boring α-proteobacterium is the etiological agent of disease in the Great Barrier Reef sponge Rhopaloeides odorabile. Mar Ecol Prog Ser 232:305–309CrossRefGoogle Scholar
  79. Webster NS, Xavier JR, Freckelton M, Motti CA, Cobb R (2008) Shifts in microbial and chemical patterns within the marine sponge Aplysina aerophoba during a disease outbreak. Environ Microbiol 10:3366–3376PubMedCrossRefGoogle Scholar
  80. Yamamoto S, Harayama S (1995) PCR amplification and direct sequencing of gyrB genes with universal primers and their application to the detection and taxonomic analysis of Pseudomonas putida strains. Appl Environ Microbiol 61:1104–1109PubMedCentralPubMedGoogle Scholar
  81. Yoon J-H, Kang S-J, Lee M-H, Oh T-K (2007) Description of Sulfitobacter donghicola sp. nov., isolated from seawater of the East Sea in Korea, transfer of Staleya guttiformis Labrenz et al. 2000 to the genus Sulfitobacter as Sulfitobacter guttiformis comb. nov. and emended description of the genus Sulfitobacter. Int J Syst Evol Microbiol 57:1788–1792PubMedCrossRefGoogle Scholar
  82. Yung PY, Kjelleberg S, Thomas T (2011) A polyphasic approach to the exploration of collagenolytic activity in the bacterial community associated with the marine sponge Cymbastela concentrica. FEMS Microbiol Lett 321:24–29PubMedCrossRefGoogle Scholar
  83. Zeng YX, Zheng TL (2011) Relationships between two Pseudoalteromonas strains isolated from the Canada Basin and the Southern Ocean using a polyphasic approach. Adv Polar Sci 22:25–34Google Scholar
  84. Zhao G-Y, Chen X-L, Zhao H-L, Xie B-B, Zhou B-C, Zhang Y-Z (2008) Hydrolysis of insoluble collagen by Deseasin MCP-01 from deep-sea Pseudoalteromonas sp. SM9913: collagenolytic characters, collagen-binding ability of C-terminal polycystic kidney disease domain, and implication for its novel role in deep-sea sedimentary particulate organic nitrogen degradation. J Biol Chem 283:36100–36107PubMedCentralPubMedCrossRefGoogle Scholar
  85. Zheng J, Leung KY (2007) Dissection of a type VI secretion system in Edwardsiella tarda. Mol Microbiol 66:1192–1206PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Jayanta D. Choudhury
    • 1
  • Arnab Pramanik
    • 1
  • Nicole S. Webster
    • 2
  • Lyndon E. Llewellyn
    • 2
  • Ratan Gachhui
    • 3
  • Joydeep Mukherjee
    • 1
    Email author
  1. 1.School of Environmental StudiesJadavpur UniversityKolkataIndia
  2. 2.Australian Institute of Marine ScienceTownsvilleAustralia
  3. 3.Department of Life Science and BiotechnologyJadavpur UniversityKolkataIndia

Personalised recommendations