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Brown Rot Syndrome and Changes in the Bacterial Сommunity of the Baikal Sponge Lubomirskia baicalensis

  • Invertebrate Microbiology
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Abstract

Mass mortality events have led to a collapse of the sponge fauna of Lake Baikal. We describe a new Brown Rot Syndrome affecting the endemic species Lubomirskia baicalensis. The main symptoms are the appearance of brown patches at the sponge surface, necrosis, and cyanobacterial fouling. 16S rRNA gene sequencing was used to characterize the bacterial community of healthy versus diseased sponges, in order to identify putative pathogens. The relative abundance of 89 eubacterial OTUs out of 340 detected has significantly changed between healthy and diseased groups. This can be explained by the depletion of host-specific prokaryotes and by the appearance and proliferation of disease-specific OTUs. In diseased sponges, the most represented OTUs belong to the families Oscillatoriaceae, Cytophagaceae, Flavobacteriaceae, Chitinophagaceae, Sphingobacteriaceae, Burkholderiaceae, Rhodobacteraceae, Comamonadaceae, Oxalobacteraceae, and Xanthomonadaceae. Although these families may contain pathogenic agents, the primary causes of changes in the sponge bacterial community and their relationship with Brown Rot Syndrome remain unclear. A better understanding of this ecological crisis will thus require a more integrative approach.

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References

  1. Wilkinson C (1987) Interocean differences in size and nutrition of coral reef sponge populations. Science 236:1654–1657. https://doi.org/10.1126/science.236.4809.1654

    Article  CAS  PubMed  Google Scholar 

  2. Diaz MC, Rützler K (2001) Sponges: an essential component of Caribbean coral reefs. Bull Mar Sci. 69(2):535–546

    Google Scholar 

  3. Hentschel U, Usher KM, Taylor MW (2006) Marine sponges as microbial fermenters. FEMS Microbiol Ecol 55(2):167–177

    Article  CAS  PubMed  Google Scholar 

  4. Webster NS (2007) Sponge disease: a global threat? Environ Microbiol 9(6):1363–1375. https://doi.org/10.1111/j.1462-2920.2007.01303.x

    Article  CAS  PubMed  Google Scholar 

  5. Webster NS, Thomas T (2016) The sponge hologenome. MBio 7(2):e00135-16. https://doi.org/10.1128/mBio.00135-16

    Article  PubMed  PubMed Central  Google Scholar 

  6. Vacelet J, Donadey C (1977) Electron microscope study of the association between some sponges and bacteria. J Exp Mar Biol Ecol 30(3):301–314

    Article  Google Scholar 

  7. Schmitt S, Tsai P, Bell J, Fromont J, Ilan M, Lindquist N, Perez T, Rodrigo A, Schupp PJ, Vacelet J, et al. (2012) Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J 6(3):564–576. https://doi.org/10.1038/ismej.2011.116

    Article  CAS  PubMed  Google Scholar 

  8. Reveillaud J, Maignien L, Murat Eren A, Huber JA, Apprill A, Sogin ML, Vanreusel A (2014) Host-specificity among abundant and rare taxa in the sponge microbiome. ISME J 8(6):1198–1209. https://doi.org/10.1038/ismej.2013.227

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Rodríguez-Marconi S, De la Iglesia R, Díez B, Fonseca CA, Hajdu E, Trefault N (2015) Characterization of bacterial, archaeal and eukaryote symbionts from Antarctic sponges reveals a high diversity at a three-domain level and a particular signature for this ecosystem. PLoS One 10(9):e0138837. https://doi.org/10.1371/journal.pone.0138837

    Article  PubMed  PubMed Central  Google Scholar 

  10. Webster NS, Luter HM, Soo RM, Botté ES, Simister RL, Abdo D, Whalan S (2013) Same, same but different: symbiotic bacterial associations in GBR sponges. Front Microbiol 3:444. https://doi.org/10.3389/fmicb.2012.00444

    Article  PubMed  PubMed Central  Google Scholar 

  11. Gernert C, Glöckner FO, Krohne G, Hentschel U (2005) Microbial diversity of the freshwater sponge Spongilla lacustris. Microb Ecol 50(2):206–212. https://doi.org/10.1007/s00248-004-0172-x

    Article  CAS  PubMed  Google Scholar 

  12. Costa R, Keller-Costa T, Gomes NC, da Rocha UN, van Overbeek L, van Elsas JD (2013) Evidence for selective bacterial community structuring in the freshwater sponge Ephydatia fluviatilis. Microb Ecol 65(1):232–244. https://doi.org/10.1007/s00248-012-0102-2

    Article  PubMed  Google Scholar 

  13. Gladkikh AS, Kaluyzhnaya OV, Belykh OI, Ahn TS, Parfenova VV (2014) Analysis of bacterial communities of two Lake Baikal endemic sponge species. Mikrobiologiia 83(6):682–693

    CAS  PubMed  Google Scholar 

  14. Seo EY, Jung D, Belykh OI, Bukshuk NA, Parfenova VV, Joung Y, Kim IC, Yim JH, Ahn T-S (2016) Comparison of bacterial diversity and species composition in three endemic Baikalian sponges. Ann Limnol 52:27–32. https://doi.org/10.1051/limn/2015035

    Article  Google Scholar 

  15. Gaino E, Pronzato R, Corriero G, Buffa P (1992) Mortality of commercial sponges: incidence in two Mediterranean areas. Boll Zool 59:79–85. https://doi.org/10.1080/11250009209386652

    Article  Google Scholar 

  16. Vacelet J, Vacelet E, Gaino E, Gallissian MF (1994) Bacterial attack of spongin skeleton during the 1986−1990 Mediterranean sponge disease. In: van Soest RWM, van Kempen TMG, Braekman JC (eds) Sponges in time and space. Balkema, Rotterdam, pp. 355–362

    Google Scholar 

  17. Perez T, Garrabou J, Sartoretto S, Harmelin J-G, Francour P, Vacelet J (2000) Mortalité massive d’invertébrés marins : un événement sans précédent en Méditerranée nord-occidentale. C.R. Acad. Sci. Paris, Sciences de la vie. Life Sci 323:853–865. https://doi.org/10.1016/S0764-4469(00)01237-3

    CAS  Google Scholar 

  18. Olson JB, Gochfeld DJ, Slattery M (2006) Aplysina red band syndrome: a new threat to Caribbean sponges. Dis Aquat Org 71(2):163–168. https://doi.org/10.3354/dao071163

    Article  CAS  PubMed  Google Scholar 

  19. 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(12):3366–3376. https://doi.org/10.1111/j.1462-2920.2008.01734.x

    Article  CAS  PubMed  Google Scholar 

  20. Garrabou J, Comaz R, Bensoussan N, Bally M, Chevaldonne P, Cigliano M, Diaz D, Harmelin JG, Gambi MC, Kersting DK, et al. (2009) Mass mortality in Northwestern Mediterranean rocky benthic communities: effects of the 2003 heat wave. Glob Chang Biol 15:1090–1103. https://doi.org/10.1111/j.1365-2486.2008.01823.x

    Article  Google Scholar 

  21. Luter HM, Whalan S, Webster NS (2010) Exploring the role of microorganisms in the disease-like syndrome affecting the sponge Ianthella basta. Appl Environ Microbiol 76(17):5736–5744. https://doi.org/10.1128/AEM.00653-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. 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 157:1577–1590. https://doi.org/10.1007/s00227-010-1431-7

    Article  Google Scholar 

  23. 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(2):218–230. https://doi.org/10.1111/j.1574-6941.2010.01001.x

    Article  CAS  PubMed  Google Scholar 

  24. 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(2):95–102. https://doi.org/10.3354/dao02460

    Article  CAS  PubMed  Google Scholar 

  25. Gao ZM, Wang Y, Tian RM, Lee OO, Wong YH, Batang ZB, Al-Suwailem A, Lafi FF, Bajic VB, Qian PY (2015) Pyrosequencing revealed shifts of prokaryotic communities between healthy and disease-like tissues of the Red Sea sponge Crella cyathophora. PeerJ 3:e890. https://doi.org/10.7717/peerj.890

    Article  PubMed  PubMed Central  Google Scholar 

  26. Sweet M, Bulling M, Cerrano C (2015) A novel sponge disease caused by a consortium of micro-organisms. Coral Reefs 34(3):871–883. https://doi.org/10.1007/s00338-015-1284-0

    Article  Google Scholar 

  27. Blanquer A, Uriz MJ, Cebrian E, Galand PE (2016) Snapshot of a bacterial microbiome shift during the early symptoms of a massive sponge die-off in the Western Mediterranean. Front Microbiol 7:752. https://doi.org/10.3389/fmicb.2016.00752

    Article  PubMed  PubMed Central  Google Scholar 

  28. Pérez T, Vacelet J (2014) Effect of climatic and anthropogenic disturbances on sponge fisheries. In: Goffredo S, Dubinsky Z (eds) The Mediterranea Sea: its history and present challenges. Springer, Dordrecht, pp. 577–587

    Chapter  Google Scholar 

  29. Harvell CD, Kim K, Burkholder JM, Colwell RR, Epstein PR, Grimes DJ, Hofmann EE, Lipp EK, Osterhaus AD, Overstreet RM, et al. (1999) Emerging marine diseases-climate links and anthropogenic factors. Science 285:1505–1510

    Article  CAS  PubMed  Google Scholar 

  30. Wulff JL (2006) Sponge systematics by starfish: predators distinguish cryptic sympatric species of Caribbean fire sponges, Tedania ignis and Tedania klausi n. sp. (Demospongiae, Poecilosclerida). Biol Bull 211:83–94. https://doi.org/10.2307/4134581

    Article  PubMed  Google Scholar 

  31. Cerrano C, Bavestrello G (2009) Massive mortalities and extinctions. In: Wahl M (ed) Marine hard bottom communities. Springer-Verlag, Berlin, pp. 295–307

    Chapter  Google Scholar 

  32. Lejeusne C, Chevaldonné P, Pergent-Martini C, Boudouresque CF, Pérez T (2010) Climate change effects on a miniature ocean: the highly diverse, highly impacted Mediterranean Sea. Trends Ecol Evol 25(4):250–260. https://doi.org/10.1016/j.tree.2009.10.009

    Article  PubMed  Google Scholar 

  33. Cebrian E, Uriz MJ, Garrabou J, Ballesteros E (2011) Sponge mass mortalities in a warming Mediterranean Sea: are cyanobacteria-harboring species worse off? PLoS One 6(6):e20211. https://doi.org/10.1371/journal.pone.0020211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. 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(3):802–813. https://doi.org/10.1007/s00248-012-0068-0

    Article  PubMed  Google Scholar 

  35. Carballo JL, Bautista E, Nava H, Cruz-Barraza JA, Chávez JA (2013) Boring sponges, an increasing threat for coral reefs affected by bleaching events. Ecol Evol 3(4):872–886. https://doi.org/10.1002/ece3.452

    Article  PubMed  PubMed Central  Google Scholar 

  36. Sokolow S (2009) Effects of a changing climate on the dynamics of coral infectious disease: a review of the evidence. Dis Aquat Org 87(1–2):5–18. https://doi.org/10.3354/dao02099

    Article  PubMed  Google Scholar 

  37. Fan L, Liu M, Simister R, Webster NS, Thomas T (2013) Marine microbial symbiosis heats up: the phylogenetic and functional response of a sponge holobiont to thermal stress. ISME J 7(5):991–1002. https://doi.org/10.1038/ismej.2012.165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Webster NS, Negri AP, Webb RI, Hill R (2002) A spongin-boring α-proteobacterium is the etiological agent of disease in the Great Barrier Reef sponge Rhopaloeides odorabile. Mar Ecol Prog Ser 232:305–309. https://doi.org/10.3354/meps232305

    Article  Google Scholar 

  39. 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 324:139–150. https://doi.org/10.3354/meps324139

    Article  CAS  Google Scholar 

  40. Galstoff PS, Brown HH, Smith CL, Smith FGW (1939) Sponge mortality in the Bahamas. Nature 143:807–808

    Article  Google Scholar 

  41. Galstoff PS (1942) Wasting disease causing mortality of sponges in the West Indies and Gulf of Mexico. Proc. 8th Amer Sci Cong 3:411–412

  42. Vacelet J, Gallissian MF (1978) Virus-like particles in cells of the sponge Verongia cavernicola (Demospongiae, Dictyoceratida) and accompanying tissue changes. J Invertebr Pathol 31:246–254

    Article  Google Scholar 

  43. Smith FGW (1939) Sponge mortality at British Honduras. Nature 144:785

    Article  Google Scholar 

  44. Sparks AK (1985) Synopsis of invertebrate pathology: exclusive of insects. Elsevier, New York

    Google Scholar 

  45. Rützler K (1988) Mangrove sponge disease induced by cyanobacterial symbionts: failure of a primitive immune system? Dis Aquat Org 5:143–149

    Article  Google Scholar 

  46. Di Camillo CG, Bartolucci I, Cerrano C, Bavestrello G (2013) Sponge disease in the Adriatic Sea. Mar. Ecol. 34:62–71. https://doi.org/10.1111/j.1439-0485.2012.00525.x

    Article  Google Scholar 

  47. Sweet M, Burn D, Croquer A, Leary P (2013) Characterisation of the bacterial and fungal communities associated with different lesion sizes of dark spot syndrome occurring in the coral Stephanocoenia intersepta. PLoS One 8(4):e62580. https://doi.org/10.1371/journal.pone.0062580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Choudhury JD, Pramanik A, Webster NS, Llewellyn LE, Gachhui R, Mukherjee J (2015) The pathogen of the Great Barrier Reef sponge Rhopaloeides odorabile is a new strain of Pseudoalteromonas agarivorans containing abundant and diverse virulence-related genes. J Mar Biotechnol (NY) 17(4):463–478. https://doi.org/10.1007/s10126-015-9627-y

    Article  CAS  Google Scholar 

  49. Efremova SM (2001) Porifera. In: Timoshkin OA (ed) An annotated list of the fauna of Lake Baikal and its catchment area. Nauka, Novosibirsk, V1, pp 177–90

  50. Kozhov MM (1972) Essays on Lake Baikal studies. Irkutsk

  51. Masuda Y (2009) Studies on the taxonomy and distribution of freshwater sponges in Lake Baikal. Prog Mol Subcell Biol 47:81–110. https://doi.org/10.1007/978-3-540-88552-8_4

    Article  PubMed  Google Scholar 

  52. Bormotov AE (2011) What has happened with Baikal sponges? Sci First Hand 5(41):20–23

    Google Scholar 

  53. Timoshkin OA, Malnik VV, Sakirko MV, Boedeker C (2014) Ecological crisis at Lake Baikal: scientists diagnose. Sci First Hand 5:75–91

    Google Scholar 

  54. Kaluzhnaya OV, Itskovich VB (2015) Bleaching of Baikalian sponge affects the taxonomic composition of symbiotic microorganisms. Genetika 51(11):1335–1340

    CAS  PubMed  Google Scholar 

  55. Timoshkin OA, Samsonov DP, Yamamuro M, Moore MV, Belykh OI, Malnik VV, Sakirko MV, Shirokaya AA, Bondarenko NA, Domysheva MV, et al. (2016) Rapid ecological change in the coastal zone of Lake Baikal (East Siberia): is the site of the world's greatest freshwater biodiversity in danger? J. Great Lakes Res. 42(3):487–497. https://doi.org/10.1016/j.jglr.2016.02.011

    Article  CAS  Google Scholar 

  56. Rezvoi PD (1936) Freshwater sponges of the USSR. In: Rezvoi PD (ed) The fauna of the USSR. Academy of Sciences, Moskow V. 2, pp 21–41

  57. Mikhailov IS, Zakharova YR, Galachyants YP, Usoltseva MV, Petrova DP, Sakirko MV, Likhoshway YV, Grachev MA (2015) Similarity of structure of taxonomic bacterial communities in the photic layer of Lake Baikal’s three basins differing in spring phytoplankton composition and abundance. Dokl Biochem Biophys 465:413–419. https://doi.org/10.1134/S1607672915060198

    Article  CAS  PubMed  Google Scholar 

  58. Semenov AD (1977) Guidance on the chemical analysis of surface waters. Gidrometeoizdat, Leningrad

    Google Scholar 

  59. Stroganov NS, Buzinova NS (1980) Practical guide in hydrochemistry. MGU, Moscow

    Google Scholar 

  60. Wetzel RG, Likens GE (1991) Limnological analyses. Springer-Verlag, New York

    Book  Google Scholar 

  61. Shimaraev MN, Domysheva VM (2013) Trends in hydrological and hydrochemical processes in Lake Baikal under conditions of modern climate change. In: Goldman CR, Kumagai M, Robarts RD (ed) Climatic change and global warming of inland waters: impacts and mitigation for ecosystems and societies. Wiley-Blackwell, pp 43–66

  62. Domysheva VM (2009) Hydrochemistry. In: Tulokhonov AK (ed) Baikal: nature and people. Ecos, Ulan-Ude, pp. 68–70

    Google Scholar 

  63. Sakirko MV, Domysheva VM, Pestunov DA, Netsvetaeva OG, Panchenko MV (2015) Concentration of nutrients in the water of Southern Baikal in summer. Proc of SPIE 9680(968045):1–7. https://doi.org/10.1117/12.2205753

    Google Scholar 

  64. Khodzher T, Domysheva VM, Sorokovikova LM et al. (2016) Methods for monitoring the chemical composition of Lake Baikal water. In: Mueller L, Sheudshen A, Eulenstein F (eds) Novel methods for monitoring and managing land and water resources in Siberia. Springer International Publishing Switzerland, pp 113–29

  65. Newton RJ, Bootsma MJ, Morrison HG (2013) A microbial signature approach to identify fecal pollution in the waters off an urbanized coast of Lake Michigan. Microb Ecol 65(4):1011–1023. https://doi.org/10.1007/s00248-013-0200-9

    Article  PubMed  PubMed Central  Google Scholar 

  66. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, et al. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537–7541. https://doi.org/10.1128/AEM.01541-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G, Ciulla D, Tabbaa D, Highlander SK, Sodergren E, et al. (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res. 21(3):494–504. https://doi.org/10.1101/gr.112730.110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucl Acids Res 41(D1):D590–D596

    Article  CAS  PubMed  Google Scholar 

  69. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072. https://doi.org/10.1128/Aem.03006-05

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. He Y, Caporaso JG, Jiang XT, Sheng HF, Huse SM, Rideout JR, Edgar RC, Kopylova E, Walters WA, Knight R, Zhou HW (2015) Stability of operational taxonomic units: an important but neglected property for analyzing microbial diversity. Microbiome 3:20. https://doi.org/10.1186/s40168-015-0081-x

    Article  PubMed  PubMed Central  Google Scholar 

  71. Kravtsova LS, Izhboldina LA, Khanaev IV, Pomazkina GV, Domysheva VM, Kravchenko OS, Grachev MA (2012) Disturbances of the vertical zoning of green algae in the coastal part of the Listvennichnyi gulf of Lake Baikal. Dokl Akad Nauk 447:227–229

    Google Scholar 

  72. Kravtsova LS, Izhboldina LA, Khanaev IV, Pomazkina GV, Rodionova EV, Domysheva VM, Sakirko MV, Tomberg IV (2014) Nearshore benthic blooms of filamentous green algae in Lake Baikal. J Great Lakes Res 40:441–448

    Article  Google Scholar 

  73. Gaikwad S, Shouche YS, Gade WN (2016) Microbial community structure of two freshwater sponges using Illumina MiSeq sequencing revealed high microbial diversity. AMB Expr 6:40. https://doi.org/10.1186/s13568-016-0211-2

    Article  Google Scholar 

  74. Vicente VP (1989) Regional commercial sponge extinction in the West Indies: are recent climatic changes responsible? Mar Ecol Prog Ser 10:179–191. https://doi.org/10.1111/j.1439-0485.1989.tb00073.x

    Article  Google Scholar 

  75. Roder C, Arif C, Daniels C (2014) Bacterial profiling of White Plague Disease across corals and oceans indicates a conserved and distinct disease microbiome. Mol Ecol 23(4):965–974. https://doi.org/10.1111/mec.12638

    Article  PubMed  PubMed Central  Google Scholar 

  76. Miller AW, Richardson LL (2011) A meta-analysis of 16S rRNA gene clone libraries from the polymicrobial black band disease of corals. FEMS Microbiol Ecol 75(2):231–241. https://doi.org/10.1111/j.1574-6941.2010.00991.x

    Article  CAS  PubMed  Google Scholar 

  77. 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(1):268–279. https://doi.org/10.1111/1574-6941.12222

    Article  CAS  PubMed  Google Scholar 

  78. Denikina NN, Dzyuba EV, Bel’kova NL, Belikov SI (2016) The first case of disease of the sponge Lubomirskia Baicalensis: investigation of its microbiome. Biol Bull 3:315–322. https://doi.org/10.7868/S0002332916030024

    Google Scholar 

  79. Kantor RS, Wrighton KC, Handley KM, Sharon I, Hug LA, Castelle CJ, Thomas BC, Banfield JF (2013) Small genomes and sparse metabolisms of sediment-associated bacteria from four candidate phyla. MBio 4(5):e00708-13. https://doi.org/10.1128/mBio.00708-13

    Article  PubMed  PubMed Central  Google Scholar 

  80. Dennis PG, Seymour J, Kumbun K, Tyson GW (2013) Diverse populations of lake water bacteria exhibit chemotaxis towards inorganic nutrients. ISME J 7(8):1661–1664. https://doi.org/10.1038/ismej.2013.47

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Kirchman DL (2002) The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiol Ecol 39(2):91–100. https://doi.org/10.1111/j.1574-6941.2002.tb00910.x

    CAS  PubMed  Google Scholar 

  82. Newton RJ, McLellan SL (2015) A unique assemblage of cosmopolitan freshwater bacteria and higher community diversity differentiate an urbanized estuary from oligotrophic Lake Michigan. Front Microbiol 6:1028. https://doi.org/10.3389/fmicb.2015.01028

    Article  PubMed  PubMed Central  Google Scholar 

  83. Liang Q, Zhang X, Lee KH, Wang Y, Yu K, Shen W, Fu L, Shu M, Li W (2015) Nitrogen removal and water microbiota in grass carp culture following supplementation with Bacillus licheniformis BSK-4. World J Microbiol Biotechnol 31(11):1711–1718. https://doi.org/10.1007/s11274-015-1921-3

    Article  CAS  PubMed  Google Scholar 

  84. Cárdenas A, Rodriguez-R LM, Pizarro V, Cadavid LF, Arévalo-Ferro C (2012) Shifts in bacterial communities of two Caribbean reef-building coral species affected by white plague disease. ISME J 6(3):502–512. https://doi.org/10.1038/ismej.2011.123

    Article  PubMed  Google Scholar 

  85. Hansen GH, Bergh O, Michaelsen J, Knappskog D (1992) Flexibacter ovolyticus sp. nov., a pathogen of eggs and larvae of Atlantic halibut, Hippoglossus hippoglossus L. Int J Syst Bacteriol 42(3):451–458. https://doi.org/10.1099/00207713-42-3-451

    Article  CAS  PubMed  Google Scholar 

  86. Declercq AM, Haesebrouck F, Van den Broeck W, Bossier P, Decostere A (2013) Columnaris disease in fish: a review with emphasis on bacterium-host interaction. Vet Res 44(1):27. https://doi.org/10.1186/1297-9716-44-27

    Article  PubMed  PubMed Central  Google Scholar 

  87. Willems A (2014) The family Comamonadaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes: Alphaproteobacteria and Betaproteobacteria, 4th edn. Springer, Berlin, pp. 777–851

    Chapter  Google Scholar 

  88. Verner-Jeffreys DW, Pond MJ, Peeler EJ, Rimmer GS, Oidtmann B, Way K, Mewett J, Jeffrey K, Bateman K, Reese RA, Feist SW (2008) Emergence of cold water strawberry disease of rainbow trout Oncorynchus mykiss in England and Wales: outbreak investigations and transmission studies. Dis Aquat Org 79(3):207–218. https://doi.org/10.3354/dao01916

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Sergey Feranchuk for bioinformatics analysis, Olga Maikova for the morphological identification, the diver Yuriy Yushchik for sampling, Natalya Bel’kova for sharing amplification primers, Maxim Khasnatinov for assistance with statistical analyses, Lubov Kravtsova and Tatyana Butina for the valuable discussion, Rachel Mackie for the English reviewing, and finally Sergey Belikov and Alexander Ereskovsky for their support.

Funding

Funding came from the Russian State Projects (0345-2016-0002, 0345-2016-0008), the Russian Foundation for Basic Research Project (16-54-150007), and the French Centre National de la Recherche Scientifique (CNRS, PRC 216483).

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Correspondence to Nina V. Kulakova.

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Kulakova, N.V., Sakirko, M.V., Adelshin, R.V. et al. Brown Rot Syndrome and Changes in the Bacterial Сommunity of the Baikal Sponge Lubomirskia baicalensis . Microb Ecol 75, 1024–1034 (2018). https://doi.org/10.1007/s00248-017-1097-5

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