Skip to main content

Advertisement

SpringerLink
Log in

The alien species Caulerpa cylindracea and its associated bacteria in the Mediterranean Sea

  • Original paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Although several studies have investigated bacterial–algal interactions, the bacterial component has often not been identified, and the ecological role of bacterial–algal associations is still unclear. In the present study two different approaches (molecular and culture) have been used to characterize the bacterial community associated with the invasive alga Caulerpa cylindracea (Sonder) over time, in a coastal area of the Mediterranean basin. C. cylindracea is an invasive macroalga in the Mediterranean Sea, able to colonize several types of substrates. Traditional culture-based and PCR-SSCP methods have been used to analyze the bacterial community. Molecular traces of Gammaproteobacteria belonging to the genera Shewanella and Vibrio have been found by both approaches on the surface of C. cylindracea consistently in time, along with those of an unknown species belonging to the Rhodobacteraceae family. Other taxa belonging to Bacillus, Pseudoalteromonas, Tropicibacter, Photobacterium, Exiguobacterium, Kocuria, Ruegeria, and Marinobacter genera have been discovered by culture-based approach. PCR-SSCP method has shown traces of an unknown species of the Bacteroidetes phylum and the Granulosicoccus genus. Our results suggest that C. cylindracea hosts a bacterial assemblage scarcely variable with time. Further studies are needed to clarify the nature of this alga–bacteria association and the potential role in the spreading of this alga using a holistic view considering the seaweed with associated bacteria as an essentially unique meta-organism.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abriouel H, Franz CM, Omar NB, Gálvez A (2011) Diversity and applications of Bacillus bacteriocins. FEMS Microbiol Rev 35(1):201–232. doi:10.1111/j.1574-6976.2010.00244.x

    Article  CAS  Google Scholar 

  • Aires T, Serrão EA, Kendrick G, Duarte CM, Arnaud-Haond S (2013) Invasion is a community affair: Clandestine followers in the bacterial community associated to green algae, Caulerpa racemosa. Track the invasion source. PLoS One 8(7):e68429. doi:10.1371/journal.pone.0068429

    Article  CAS  Google Scholar 

  • Ashen JB, Goff LJ (1996) Molecular identification of a bacterium associated with gall formation in the marine red alga Prionitis lanceolata. J Phycol 32:286–297. doi:10.1111/j.0022-3646.1996.00286.x

    Article  CAS  Google Scholar 

  • Ast JC, Cleenwerck I, Engelbeen K, Urbanczyk H, Thompson FL, De Vos P, Dunlap PV (2007) Photobacterium kishitanii sp. nov., a luminous marine bacterium symbiotic with deep-sea fishes. Int J Syst Evol Microbiol 57:2073–2078. doi:10.1099/ijs.0.65153-0

    Article  CAS  Google Scholar 

  • Baumann P, Baumann L, Bang SS, Woolkalis MJ (1980) Reevaluation of the taxonomy of Vibrio, Beneckea, and Photobacterium: abolition of the genus Beneckea. Curr Microbiol 4(3):127–132. doi:10.1007/BF02602814

    Article  Google Scholar 

  • Belton GS, Prud’homme van Reine WF, Huisman JM, Draisma SGA, Gurgel CFD (2014) Resolving phenotypic plasticity and species designation in the morphology challenging Caulerpa racemosa-peltata complex (Caulerpaceae, Chlorophyta). J Phycol 50(1):32–54. doi:10.1111/jpy.12132

    Article  CAS  Google Scholar 

  • Bengtsson MM, Sjøtun K, Lanzén A, Øvreås L (2012) Bacterial diversity in relation to secondary production and succession on surfaces of the kelp Laminaria hyperborea. ISME J 6(12):2188–2198. doi:10.1038/ismej.2012.67

    Article  CAS  Google Scholar 

  • Bernbom N, Ng YY, Olsen SM, Gram L (2013) Pseudoalteromonas spp. serve as initial bacterial attractants in mesocosms of coastal waters but have subsequent antifouling capacity in mesocosms and when embedded in paint. Appl Environ Microbiol 79(22):6885–6893. doi:10.1128/AEM.01987-13

    Article  CAS  Google Scholar 

  • Burke C, Steinberg P, Rusch D, Kjelleberg S, Thomas T (2011a) Bacterial community assembly based on functional genes rather than species. Proc Natl Acad Sci USA 108:14288–14293. doi:10.1073/pnas.1101591108

    Article  CAS  Google Scholar 

  • Burke C, Thomas T, Lewis M, Steinberg P, Kjelleberg S (2011b) Composition, uniqueness and variability of the epiphytic bacterial community of the green alga Ulva australis. ISME J 5:590–600. doi:10.1038/ismej.2010.164

    Article  CAS  Google Scholar 

  • Cano-Gómez A, Goulden EF, Owens L, Høj L (2010) Vibrio owensii sp. nov., isolated from cultured crustaceans in Australia. FEMS Microbiol Lett 302(2):175–181. doi:10.1111/j.1574-6968.2009.01850.x

    Article  Google Scholar 

  • Cebrian E, Linares C, Marchal C, Garrabou J (2012) Exploring the effects of invasive algae on the persistence of gorgonian populations. Biol Invasions 14:2647–2656. doi:10.1007/s10530-012-0261-6

    Article  Google Scholar 

  • Chimetto LA, Cleenwerck I, Alves N, Silva BS, Brocchi M, Willems A, De Vos P, Thompson FL (2011) Vibrio communis sp. nov., isolated from the marine animals Mussismilia hispida, Phyllogorgia dilatata, Palythoa caribaeorum, Palythoa variabilis and Litopenaeus vannamei. Int J Syst Evol Microbiol 61(2):362–368. doi:10.1099/ijs.0.019729-0

    Article  CAS  Google Scholar 

  • Dheilly A, Soum-Soutéra E, Klein GL, Bazire A, Compére C, Haras D, Dufour A (2010) Antibiofilm activity of the marine bacterium Pseudoalteromonas sp. strain 3J6. Appl Environ Microbiol 76:3452–3461. doi:10.1128/AEM.02632-09

    Article  CAS  Google Scholar 

  • Dobretsov SV, Dahms HU, Harder T, Qian PY (2006) Allelochemical defense against epibiosis in the macroalga Caulerpa racemosa var. turbinata. Mar Ecol Prog Ser 318:165–175. doi:10.3354/meps318165

    Article  CAS  Google Scholar 

  • Editorial (2013) The cultural revolution. Nat Rev Microbiol 11:1. doi:10.1038/nrmicro2948

    Google Scholar 

  • Egan S, Thomas T, Holmstrom C, Kjelleberg S (2000) Phylogenetic relationship and antifouling activity of bacterial epiphytes from the marine alga Ulva lactuca. Environ Microbiol 2:343–347. doi:10.1046/j.1462-2920.2000.00107.x

    Article  CAS  Google Scholar 

  • Felline S, Caricato R, Cutignano A, Gorbi S, Lionetto MG, Mollo E, Regoli F, Terlizzi A (2012) Subtle effects of biological invasions: cellular and physiological responses of fish eating the exotic pest Caulerpa racemosa. PLoS One 7:e38763. doi:10.1371/journal.pone.0038763

    Article  CAS  Google Scholar 

  • Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376. doi:10.1007/BF01734359

    Article  CAS  Google Scholar 

  • Gauthier G, Gauthier M, 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 Bacteriol 45:755–761. doi:10.1099/00207713-45-4-755

    Article  CAS  Google Scholar 

  • Goecke F, Labes A, Wiese J, Imhoff JF (2010) Chemical interactions between marine macroalgae and bacteria. Mar Ecol Prog Ser 409:267–299. doi:10.3354/meps08607

    Article  CAS  Google Scholar 

  • Goecke F, Labes A, Wiese J, Imhoff JF (2013a) Phylogenetic analysis and antibiotic activity of bacteria isolated from the surface of two co-occurring macroalgae from the Baltic Sea. Eur J Phycol 48(1):47–60. doi:10.1080/09670262.2013.767944

    Article  Google Scholar 

  • Goecke F, Thiel V, Wiese J, Labes A, Imhoff JF (2013b) Algae as an important environment for bacteria: phylogenetic relationships among new bacterial species isolated from algae. Phycologia 52:14–24. doi:10.2216/12-24.1

    Article  CAS  Google Scholar 

  • Gomez-Gil B, Thompson FL, Thompson CC, Swings J (2003) Vibrio rotiferianus sp. nov., isolated from cultures of the rotifer Brachionus plicatilis. Int J Syst Evol Microbiol 53(1):239–243. doi:10.1099/ijs.0.02430-0

    Article  CAS  Google Scholar 

  • Goulden EF, Hall MR, Bourne DG, Pereg LL, Høj L (2012) Pathogenicity and infection cycle of Vibrio owensii in larviculture of the ornate spiny lobster (Panulirus ornatus). Appl Environ Microbiol 78(8):2841–2849. doi:10.1128/AEM.07274-11

    Article  CAS  Google Scholar 

  • Gouy M, Guindon S, Gascuel O (2010) SeaView Version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27(2):221–224. doi:10.1093/molbev/msp259

    Article  CAS  Google Scholar 

  • Guerrero-Ferreira R, Gorman C, Chavez AA, Willie S, Nishiguchi MK (2013) Characterization of the bacterial diversity in Indo-West Pacific loliginid and sepiolid squid light organs. Microb Ecol 65(1):214–226. doi:10.1007/s00248-012-0099-6

    Article  CAS  Google Scholar 

  • Hollants J, Leroux O, Leliaert F, Decleyre H, De Clerck O, Willems A (2011) Who is in there? Exploration of endophytic bacteria within the siphonous green seaweed Bryopsis (Bryopsidales, Chlorophyta). PLoS One 6(10):e26458. doi:10.1371/journal.pone.0026458

    Article  CAS  Google Scholar 

  • Holmström C, Egan S, Franks A, McCloy S, Hjelleberg S (2002) Antifouling activities expressed by marine surface associated Pseudoalteromonas species. FEMS Microbiol Ecol 41:47–58. doi:10.1111/j.1574-6941.2002.tb00965.x

    Article  Google Scholar 

  • Ivanova EP, Nedashkovskaya OI, Zhukova NV, Nicolau DV, Christen R, Mikhailov VV (2003) Shewanella waksmanii sp. nov., isolated from a sipuncula (Phascolosoma japonicum). Int J Syst Evol Microbiol 53(5):1471–1477. doi:10.1099/ijs.0.02630-0

    Article  CAS  Google Scholar 

  • Kim IG, Lee MH, Jung SY, Song JJ, Oh TK, Yoon JH (2005) Exiguobacterium aestuarii sp. nov. and Exiguobacterium marinum sp. nov., isolated from a tidal flat of the Yellow Sea in Korea. Int J Syst Evol Microbiol 55(2):885–889. doi:10.1099/ijs.0.63308-0

    Article  CAS  Google Scholar 

  • Kim YO, Kim KK, Park S, Kang SJ, Lee JH, Lee SJ, Oh TK, Yoon JH (2010) Photobacterium gaetbulicola sp. nov., a lipolytic bacterium isolated from a tidal flat sediment. Int J Syst Evol Microbiol 60(11):2587–2591. doi:10.1099/ijs.0.016923-0

    Article  CAS  Google Scholar 

  • Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park SC, Jeon YS, Lee JH, 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 62:716–721. doi:10.1099/ijs.0.038075-0

    Article  CAS  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120. doi:10.1007/BF01731581

    Article  CAS  Google Scholar 

  • Klein J, Verlaque M (2008) The Caulerpa racemosa invasion: a critical review. Mar Pollut Bull 56:205–225. doi:10.1016/j.marpolbul.2007.09.043

    Article  CAS  Google Scholar 

  • Kurilenko VV, Christen R, Zhukova NV, Kalinovskaya NI, Mikhailov VV, Crawford RJ, Ivanova EP (2010) Granulosicoccus coccoides sp. nov., isolated from leaves of seagrass (Zostera marina). Int J Syst Evol Microbiol 60(4):972–976. doi:10.1099/ijs.0.013516-0

    Article  Google Scholar 

  • Lachnit T, Meske D, Wahl M, Harder T, Schmitz R (2011) Epibacterial community patterns on marine macroalgae are host-specific but temporally variable. Environ Microbiol 13:655–665. doi:10.1111/j.1462-2920.2010.02371.x

    Article  Google Scholar 

  • Lane DJ, Pace B, Olsen GJ, Stahl DA, Sogin ML, Pace NR (1985) Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc Natl Acad Sci USA 82:6955–6959. doi:10.1073/pnas.82.20.6955

    Article  CAS  Google Scholar 

  • Lee K, Lee HK, Choi T-H, Kim K-MT, Cho J-C (2007) Granulosicoccaceae fam. nov., to include Granulosicoccus antarcticus gen. nov., sp. nov., a non-phototrophic, obligately aerobic chemoheterotroph in the order Chromatiales, isolated from antarctic Seawater. J Microbiol Biotechnol 17:1483–1490

    CAS  Google Scholar 

  • Lee OO, Lai PY, Wu HX, Zhou XJ, Miao L, Wang H, Qian PY (2012) Marinobacter xestospongiae sp. nov., isolated from the marine sponge Xestospongia testudinaria collected from the Red Sea. Int J Syst Evol Microbiol 62(8):1980–1985. doi:10.1099/ijs.0.028811-0

    Article  CAS  Google Scholar 

  • Lenk S, Moraru C, Hahnke S, Arnds J, Richter M, Kube M, Reinhardt R, Brinkhoff Harder TJ, Amann R, Mußmann M (2012) Roseobacter clade bacteria are abundant in coastal sediments and encode a novel combination of sulfur oxidation genes. ISME J 6(12):2178–2187. doi:10.1038/ismej.2012.66

    Article  CAS  Google Scholar 

  • Longford SR, Tujula NA, Crocetti GR, Holmes AJ, Holmström C, Kjelleberg S, Steinberg PD, Taylor MW (2007) Comparisons of diversity of bacterial communities associated with three sessile marine eukaryotes. Aquat Microb Ecol 48:217–229. doi:10.3354/ame048217

    Article  Google Scholar 

  • Lucena T, Pujalte MJ, Ruvira MA, Garay E, Macián MC, Arahal DR (2012) Tropicibacter multivorans sp. nov., an aerobic alphaproteobacterium isolated from surface seawater. Int J Syst Evol Microbiol 62(4):844–848. doi:10.1099/ijs.0.030973-0

    Article  CAS  Google Scholar 

  • MacDonell MT, Colwell RR (1985) Phylogeny of the Vibrionaceae, and recommendation for two new genera, Listonella and Shewanella. Syst Appl Microbiol 6:171–182

    Article  CAS  Google Scholar 

  • Martin M, Portetelle D, Michel G, Vandenbol M (2014) Microorganisms living on macroalgae: diversity, interactions, and biotechnological applications. Appl Microbiol Biotechnol 98(7):2917–2935. doi:10.1007/s00253-014-5557-2

    Article  CAS  Google Scholar 

  • Meusnier I, Olsen JL, Stam WT, Destombe C, Valero M (2001) Phylogenetic analyses of Caulerpa taxifolia (Chlorophyta) and of its associated bacterial microflora provide clues to the origin of the Mediterranean introduction. Mol Ecol 10(4):931–946. doi:10.1046/j.1365-294X.2001.01245.x

    Article  CAS  Google Scholar 

  • Myers CR, Nealson KH (1988) Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor. Science 240:1319–1321. doi:10.1126/science.240.4857.1319

    Article  CAS  Google Scholar 

  • Nocker A, Burr M, Camper AK (2007) Genotypic microbial community profiling: a critical technical review. Microb Ecol 54(2):276–289. doi:10.1007/s00248-006-9199-5

    Article  CAS  Google Scholar 

  • Park S, Yoon JH (2012) Ruegeria arenilitoris sp. nov., isolated from the seashore sand around a seaweed farm. Antonie Van Leeuwenhoek 102(4):581–589. doi:10.1007/s10482-012-9753-8

    Article  Google Scholar 

  • Petrovskis EA, Vogel TM, Adriaens P (1994) Effects of electron acceptors and donors on transformation of tetrachloromethane by Shewanella putrefaciens MR-1. FEMS Microbiol Lett 121:357–364. doi:10.1111/j.1574-6968.1994.tb07126.x

    Article  CAS  Google Scholar 

  • Piazzi L, Ceccherelli G, Cinelli F (2001) Threat to macroalgal diversity: effects of the introduced green alga Caulerpa racemosa in the Mediterranean. Mar Ecol Prog Ser 210:161–165. doi:10.3354/meps210149

    Article  Google Scholar 

  • Porter KG, Feig YS (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25:943–948

    Article  Google Scholar 

  • Prado S, Romalde JL, Montes J, Barja JL (2005) Pathogenic bacteria isolated from disease outbreaks in shellfish hatcheries: first description of Vibrio neptunius as an oyster pathogen. Dis Aquat Organ 67:209–215. doi:10.3354/dao067209

    Article  CAS  Google Scholar 

  • Preston GM, Haubold B, Rainey PR (1998) Bacterial genomics and adaptation to life on plants: implications for the evolution of pathogenicity and symbiosis. Curr Opin Microbiol 1:589–597. doi:10.1016/S1369-5274(98)80094-5

    Article  CAS  Google Scholar 

  • Rivas R, Garcıa-Fraile P, Mateos PF, Martınez-Molina E, Velazquez E (2006) Photobacterium halotolerans sp. nov., isolated from Lake Martel in Spain. Int J Syst Evol Microbiol 56:1067–1071. doi:10.1099/ijs.0.64099-0

    Article  CAS  Google Scholar 

  • Ruitton S, Verlaque M, Boudouresque CF (2005) Seasonal changes of the introduced Caulerpa racemosa var. cylindracea (Caulerpales, Chlorophyta) at the northwest limit of its Mediterranean distribution. Aquat Bot 82:55–70. doi:10.1016/j.aquabot.2005.02.008

    Article  Google Scholar 

  • Russell NJ, Nichols DS (1999) Polyunsaturated fatty acids in marine bacteria: a dogma rewritten. Microbiology 145:767–779

    Article  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbour-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  Google Scholar 

  • Salemi M, Vandamme AM (2003) The phylogenetic handbook: a practical approach to DNA and protein phylogeny. Cambridge University Press, Cambridge

    Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbour Laboratory Press, New York

    Google Scholar 

  • Sauvage T, Payri C, Draisma SGA, van Reine WFPH, Verbruggen H, Belton GS, Gurgel CFD, Gabriel D, Sherwood AR, Fredericq S (2013) Molecular diversity of the Caulerpa racemosa–Caulerpa peltata complex (Caulerpaceae, Bryopsidales) in New Caledonia, with new Australasian records for C. racemosa var. cylindracea. Phycologia 52(1):6–13. doi:10.2216/11-116.1

    Article  Google Scholar 

  • Schumann P, Spröer C, Burghardt J, Kovacs G, Stackebrandt E (1999) Reclassification of the species Kocuria erythromyxa (Brooks and Murray 1981) as Kocuria rosea (Flügge 1886). Int J Syst Bacteriol 49(2):393–396

    Article  Google Scholar 

  • Schumann P, Tindall BJ, Mendrock U, Kramer I, Stackebrandt E (2000) Pelczaria aurantia ATCC 49321T (=DSM 12801T) is a strain of Kocuria rosea (Flügge 1886) Stackebrandt et al. 1995. Int J Syst Evol Microbiol 50(4):1421–1424

    Article  CAS  Google Scholar 

  • Semple KM, Westlake DWS (1987) Characterization of iron reducing Alteromonas putrefaciens strains from oil field fluids. Can J Microbiol 35:925–931

    Article  Google Scholar 

  • Seo HJ, Bae SS, Lee JH, Kim SJ (2005) Photobacterium frigidiphilum sp. nov., a psychrophilic, lipolytic bacterium isolated from deep-sea sediments of Edison Seamount. Int J Syst Evol Microbiol 55:1661–1666. doi:10.1099/ijs.0.63338-0

    Article  CAS  Google Scholar 

  • Shade A, Hogan CS, Klimowicz AK, Linske M, McManus PS, Handelsman J (2012) Culturing captures members of the soil rare biosphere. Environ Microbiol 14(9):2247–2252. doi:10.1111/j.1462-2920.2012.02817.x

    Article  Google Scholar 

  • Singh RP, Reddy CRK (2014) Seaweed–microbial interactions: key functions of seaweed-associated bacteria. FEMS Microbiol Ecol 88(2):213–230. doi:10.1111/1574-6941.12297

    Article  CAS  Google Scholar 

  • Slepecky RA, Hemphill HE (2006) The genus Bacillus: nonmedical. In: Dworkin M, Falkow S (eds) The prokaryotes: bacteria: firmicutes, cyanobacteria, vol 4. Springer Science & Business Media, New York, pp 530–562. doi:10.1007/0-387-30744-3_16

    Google Scholar 

  • Sober E (1983) Parsimony in systematics: philosophical issues. Annu Rev Ecol Evol Syst 14:335–357

    Article  Google Scholar 

  • Stabili L, Gravili C, Tredici SM, Piraino S, Talà A, Boero F, Alifano P (2008) Epibiotic Vibrio luminous bacteria isolated from some Hydrozoa and Bryozoa species. Microb Ecol 56(4):625–636

    Article  CAS  Google Scholar 

  • Stabili L, Rizzo L, Alifano P, Fraschetti S (2014) Functional diversity of the bacterial community associated to the invasive alien seaweed Caulerpa racemosa. Biol Mar Mediterr 21(1):127–128

    Google Scholar 

  • Staufenberger T, Thiel V, Wiese J, Imhoff JF (2008) Phylogenetic analysis of bacteria associated with Laminaria saccharina. FEMS Microbiol Ecol 64:65–77. doi:10.1111/j.1574-6941.2008.00445.x

    Article  CAS  Google Scholar 

  • Talà A, Lenucci M, Gaballo A, Durante M, Tredici SM, Debowles DA, Pizzolante G, Marcuccio C, Carata E, Piro G, Carpita NC, Mita G, Alifano P (2013) Sphingomonas cynarae sp. nov., a proteobacterium that produces an unusual type of sphingan. Int J Syst Evol Microbiol 63:72–79. doi:10.1099/ijs.0.032060-0

    Article  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680. doi:10.1093/nar/22.22.4673

    Article  CAS  Google Scholar 

  • Thompson FL, Li Y, Gomez-Gil B, Thompson CC, Hoste B, Vandemeulebroecke K, Rupp GS, Pereira A, De Bem MM, Sorgeloos P, Swings J (2003) Vibrio neptunius sp. nov., Vibrio brasiliensis sp. nov. and Vibrio xuii sp. nov., isolated from the marine aquaculture environment (bivalves, fish, rotifers and shrimps). Int J Syst Evol Microbiol 53(1):245–252. doi:10.1099/ijs.0.02447-0

    Article  CAS  Google Scholar 

  • Thompson FL, Thompson CC, Naser S, Hoste B, Vandemeulebroecke K, Munn C, Bourne D, Swings J (2005) Photobacterium rosenbergii sp. nov. and Enterovibrio coralii sp. nov., vibrios associated with coral bleaching. Int J Syst Evol Microbiol 55:913–917. doi:10.1099/ijs.0.63370-0

    Article  CAS  Google Scholar 

  • Urbanczyk H, Yoshitoshi O, Hayashi T (2013) Taxonomic revision of Harveyi clade bacteria (family Vibrionaceae) based on analysis of whole genome sequences. Int J Syst Evol Microbiol 63(7):2742–2751. doi:10.1099/ijs.0.051110-0

    Article  Google Scholar 

  • 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(2):565–574. doi:10.1099/00207713-50-2-565

    Article  CAS  Google Scholar 

  • 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 49:705–724. doi:10.1099/00207713-49-2-705

    Article  CAS  Google Scholar 

  • Verlaque M, Durand C, Huisman JM, Boudouresque CF, Le Parco Y (2003) On the identity and origin of the Mediterranean invasive Caulerpa racemosa (Caulerpales, Chlorophyta). Eur J Phycol 38:325–339. doi:10.1080/09670260310001612592

    Article  Google Scholar 

  • Wahl M, Goecke F, Labes A, Dobretsov S, Weinberger F (2012) The second skin: ecological role of epibiotic biofilms on marine organisms. Front Microbiol 3:292. doi:10.3389/fmicb.2012.00292

    Article  CAS  Google Scholar 

  • Wichard T (2015) Exploring bacteria-induced growth and morphogenesis in the green macroalga order Ulvales (Chlorophyta). Front Plant Sci. doi:10.3389/fpls.2015.00086

    Google Scholar 

  • Xiao P, Jiang M, Liu Y, Sun M, Zhang L, Jie L, Li G, Mo Z (2015) Splenic necrosis signs and pathogen detection in cultured half-smooth tongue sole, Cynoglossus semilaevis Günther. J Fish Dis 38(1):103–106. doi:10.1111/jfd.12213

    Article  CAS  Google Scholar 

  • Yoon JH, Oh TK (2005) Bacillus litoralis sp. nov., isolated from a tidal flat of the Yellow Sea in Korea. Int J Syst Evol Microbiol 55(5):1945–1948. doi:10.1099/ijs.0.63332-0

    Article  CAS  Google Scholar 

  • Yoshizawa S, Tsuruya Y, Fukui Y, Sawabe T, Yokota A, Kogure K, Higgins M, Carson J, Thompson FL (2012) Vibrio jasicida sp. nov., a member of the Harveyi clade, isolated from marine animals (packhorse lobster, abalone and Atlantic salmon). Int J Syst Evol Microbiol 62(8):1864–1870. doi:10.1099/ijs.0.025916-0

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Financial support was provided by RITMARE Flagship Project and by the PRIN TETRIS funded by the Italian Ministry of University and Research. The European Community’s 7th Framework Programmes (FP7/2007–2013) for the project COCONET (Grant agreement No. 287844, http://www.coconet-fp7.eu/) and PERSEUS (Grant agreement No. 287600, http://www.perseus-net.eu/site/content.php) are also acknowledged. Christian Vaglio and the staff of the Marine Protected Area of Torre Guaceto helped in the field. Thanks are due to Dr. Maurizio Salvatore Tredici and Dr. Marco Lezzi for the support in the laboratory.

Author information

Authors and Affiliations

  1. Dipartimento di Scienze e Tecnologie Biologiche ed Ambientali, Università del Salento, CoNISMa, Via Prov.le Lecce Monteroni, Lecce, Italy

    Lucia Rizzo, Simonetta Fraschetti, Pietro Alifano, Graziano Pizzolante & Loredana Stabili

  2. Dipartimento di Scienze Ambientali, Informatica e Statistica, Università Ca’ Foscari di Venezia, Venice, Italy

    Lucia Rizzo

  3. Istituto per l’Ambiente Marino Costiero, U.O.S. di Taranto, CNR, Via Roma 3, Taranto, Italy

    Loredana Stabili

Authors
  1. Lucia Rizzo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Simonetta Fraschetti
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pietro Alifano
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Graziano Pizzolante
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Loredana Stabili
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lucia Rizzo.

Additional information

Responsible Editor: F. Weinberger.

Reviewed by T. Aires and an undisclosed expert.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rizzo, L., Fraschetti, S., Alifano, P. et al. The alien species Caulerpa cylindracea and its associated bacteria in the Mediterranean Sea. Mar Biol 163, 4 (2016). https://doi.org/10.1007/s00227-015-2775-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-015-2775-9

Keywords

Search

Navigation