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The bacterial community associated with Tetraselmis suecica outdoor mass cultures

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Abstract

Interactions between algae and associated bacterial communities in the phycosphere depend on many factors such as culture age, nutrient availability, and antibiotic production and greatly influence algal survival and growth. The microbial community associated with the marine microalga Tetraselmis suecica F&M-M33 in a laboratory culture and an outdoor mass culture, set up from the laboratory one, run during a whole year was investigated in different seasons through isolation in pure culture of bacteria, amplified ribosomal DNA restriction analysis (ARDRA) of all the isolates, and terminal restriction fragment length polymorphism (T-RFLP) analysis. The total number of bacterial isolates was 152, which clustered in thirty-six 16S rDNA groups by ARDRA. Sequencing of a representative of each ARDRA group permitted identification of bacterial genera never reported before in association with microalgae in outdoor mass cultures, although most of them were previously found to be associated with the marine environment (e.g., seawater, sea sediments). T-RFLP analysis revealed that spring and autumn bacterial community profiles were closely related, while the bacterial laboratory community was considerably different (less than 50 % similarity) from that associated with the outdoor culture in different seasons. T-RFLP results suggest the presence of a core of bacteria that are closely associated with the alga and of a part of the community which varies seasonally.

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References

  • Allgaier M, Uphoff H, Felske A, Wagner-Döbler I (2003) Aerobic anoxygenic photosynthesis in Roseobacter clade bacteria from diverse marine habitats. Appl Environ Microb 69:5051–5059

    Article  CAS  Google Scholar 

  • Amin SA, Green DH, Hart MC, Kupper FC, Sundac WG, Carrano CJ (2009) Photolysis of iron–siderophore chelates promotes bacterial–algal mutualism. Proc Natl Acad Sci U S A 106:17071–17076

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amin SA, Hmelo LR, van Tol HM, Durham BP, Carlson LT, Heal KR, Morales RL, Berthiaume CT, Parker MS, Djunaedi B, Ingalls AE, Parsek MR, Moran MA, Armbrust EV (2015) Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 522:98–101

    Article  CAS  PubMed  Google Scholar 

  • AquaFUELs (2011) Taxonomy, Biology and Biotechnology. Report of the AquaFUELs Project. www.aquafuels.eu/attachments/079_Merged%20reports%20-Taxonomy_Biology%20&%20Biotechnology.pdf. Accessed 14 Nov 1912.

  • Arora M, Chandrashekar Anil A, Delany J, Rajarajan N, Emami K, Mesbahi E (2012) Carbohydrate degrading bacteria closely associated with Tetraselmis indica: influence on algal growth. Aquat Biol 15:61–71

    Article  Google Scholar 

  • Austin B, Baudet E, Stobie M (1992) Inhibition of bacterial fish pathogens by Tetraselmis suecica. J Fish Dis 15:55–61

    Article  Google Scholar 

  • Azam F, Malfatti F (2007) Microbial structuring of marine ecosystems. Nat Rev Microbiol 5:782–791

    Article  CAS  PubMed  Google Scholar 

  • Baker KH, Herson DS (1978) Interactions between the diatom Thalassiosira pseudonanna and an associated pseudomonad in a mariculture system. Appl Environ Microb 35:791–796

  • Bell W, Mitchell R (1972) Chemotactic and growth responses of marine bacteria to algal extracellular products. Biol Bull 143:265–277

    Article  Google Scholar 

  • Berg GM, Repeta DJ, Laroche J (2002) Dissolved organic nitrogen hydrolysis rates in axenic cultures of Aureococcus anophagefferens (Pelagophyceae): comparison with heterotrophic bacteria. Appl Environ Microb 68:401–404

    Article  CAS  Google Scholar 

  • Bondioli P, Della Bella L, Rivolta G, Chini Zittelli G, Bassi N, Rodolfi L, Casini D, Prussi M, Chiramonti D, Tredici MR (2012) Oil production by the marine microalgae Nannochloropsis sp. F&M-M24 and Tetraselmis suecica F&M-M33. Bioresource Technol 114:567–572

    Article  CAS  Google Scholar 

  • Bruckner CG, Bahulikar R, Rahalkar M, Schink B, Kroth PG (2008) Bacteria associated with benthic diatoms from Lake Constance: phylogeny and influences on diatom growth and secretion of extracellular polymeric substances. Appl Environ Microb 74:7740–7749

    Article  CAS  Google Scholar 

  • Buchan A, González JM, Moran MA (2005) Overview of the marine Roseobacter lineage. Appl Environ Microb 71:5665–5677

    Article  CAS  Google Scholar 

  • Chini Zittelli G, Pastorelli R, Tredici MR (2000) A Modular Flat Panel Photobioreactor (MFPP) for indoor cultivation of Nannochloropsis sp. under artificial illumination. J Appl Phycol 12:521–526

    Article  Google Scholar 

  • Chini Zittelli G, Rodolfi L, Biondi N, Tredici MR (2006) Productivity and photosynthetic efficiency of outdoor cultures of Tetraselmis suecica in annular columns. Aquaculture 261:932–943

    Article  Google Scholar 

  • Chini Zittelli G, Rodolfi L, Bassi N, Biondi N, Tredici MR (2013a) Photobioreactors for microalgae biofuel production. In: Borowitzka MA, Moheimani N (eds) Algae for biofuels and energy. Springer, Dordrecht, pp 115–131

    Chapter  Google Scholar 

  • Chini Zittelli G, Biondi N, Rodolfi L, Tredici MR (2013b) Photobioreactors for mass production of microalgae. In: Richmond A, Hu Q (eds) Handbook of microalgal culture: applied phycology and biotechnology, 2nd edn. Wiley, Oxford, pp 225–266

    Chapter  Google Scholar 

  • Cole JJ (1982) Interactions between bacteria and algae in aquatic ecosystems. Annu Rev Ecol Syst 13:291–314

    Article  Google Scholar 

  • Dakhama A, de la Noüe J, Lavoie MC (1993) Isolation and identification of antialgal substances produced by Pseudomonas aeruginosa. J Appl Phycol 5:297–306

    Article  CAS  Google Scholar 

  • Fukami K, Nishijima T, Ishida Y (1997) Stimulative and inhibitory effects of bacteria on the growth of microalgae. Hydrobiologia 358:185–191

    Article  Google Scholar 

  • Global Catalogue of Microorganisms, http://gcm.wfcc.info/Strain_numberToInfoServlet?strain_number=NBRC%20101843. Accessed 13 July 2016

  • Green DH, Llewellyn LE, Negri AP, Blackburn SI, Bolch CJS (2004) Phylogenetic and functional diversity of the cultivable bacterial community associated with the paralytic shellfish poisoning dinoflagellate Gymnodinium catenatum. FEMS Microbiol Ecol 47:345–357

    Article  CAS  PubMed  Google Scholar 

  • Green DH, Shenoy DM, Hart MC, Hatton AD (2011) Coupling of dimethylsulfide oxidation to biomass production by a marine Flavobacterium. Appl Environ Microb 77:3137–3140

    Article  CAS  Google Scholar 

  • Grossart HP, Simon M (2007) Interactions of planktonic algae and bacteria: effects on algal growth and organic matter dynamics. Aquat Microb Ecol 47:163–176

    Article  Google Scholar 

  • Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana (Hustedt) and Detonula confervacea (Cleve). Can J Microbiol 8:229–239

    Article  CAS  PubMed  Google Scholar 

  • Hold GL, Smith EA, Birkbeck TH, Gallacher S (2001) Comparison of Paralytic Shellfish Toxin (PST) production by the dinoflagellates Alexandrium lusitanicum NEPCC 253 and Alexandrium tamarense NEPCC 407 in the presence and absence of bacteria. FEMS Microbiol Ecol 36:223–234

  • Huang S, Fulbright S, Zeng X, Yates T, Wardle G, Chisholm S, Xu J, Lammers P (2011) Characterization of the bacterial metagenome in an industrial algae bioenergy production system. Poster presented at the 4th Congress of the International Society for Applied Phycology, Halifax, Canada, 19-24/06/2011. http://www.osti.gov/scitech/servlets/purl/1093676. Accessed 26 September 2016

  • Hulatt CJ, Thomas DN (2010) Dissolved organic matter (DOM) in microalgal photobioreactors: a potential loss in solar energy conversion? Bioresour Technol 101:8690–8697

  • Hwang CY, Cho BC (2008) Ponticoccus litoralis gen. nov., sp. nov., a marine bacterium in the family Rhodobacteraceae. Int J Syst Evol Micr 58:1332–1338

    Article  CAS  Google Scholar 

  • Hwang CY, Zhang GI, Kang S-H, Kim HJ, Cho BC (2009) Pseudomonas pelagia sp. nov., isolated from a culture of the Antarctic green alga Pyramimonas gelidicola. Int J Syst Evol Micr 59:3019–3024

    Article  CAS  Google Scholar 

  • Irianto A, Austin B (2002) Probiotics in aquaculture. J Fish Dis 25:633–642

    Article  Google Scholar 

  • Jasti S, Sieracki ME, Poulton NJ, Giewat MW, Rooney-Varga JN (2005) Phylogenetic diversity and specificity of bacteria closely associated with Alexandrium spp. and other phytoplankton. Appl Environ Microb 71:3483–3494

    Article  CAS  Google Scholar 

  • Kaczmarska I, Ehrman JM, Bates SS, Green DH, Léger C, Harris J (2005) Diversity and distribution of epibiotic bacteria on Pseudo-nitzschia multiseries (Bacillariophyceae) in culture, and comparison with those on diatoms in native seawater. Harmful Algae 4:725–741

    Article  Google Scholar 

  • Kim B-S, Kim O-S, Moon EY, Chun J (2010) Vitellibacter aestuarii sp. nov., isolated from tidal-flat sediment, and an emended description of the genus Vitellibacter. Int J Syst Evol Micr 60:1989–1992

    Article  CAS  Google Scholar 

  • Kirchman DL (2002) The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiol Ecol 39:91–100

    CAS  PubMed  Google Scholar 

  • Kohli GS, John U, Figueroa RI, Rhodes LL, Harwood DT, Groth M, Bolch CJS, Murray SA (2015) Polyketide synthesis genes associated with toxin production in two species of Gambierdiscus (Dinophyceae). BMC Genomics 16:410

    Article  PubMed  PubMed Central  Google Scholar 

  • Kuo RC, Lin S (2013) Ectobiotic and endobiotic bacteria associated with Eutreptiella sp. isolated from Long Island Sound. Protist 164:60–74

    Article  PubMed  Google Scholar 

  • Lakaniemi A-M, Intihar VM, Tuovinen OH, Puhakka JA (2012a) Growth of Chlorella vulgaris and associated bacteria in photobioreactors. Microb Biotechnol 5:69–78

    Article  CAS  PubMed  Google Scholar 

  • Lakaniemi A-M, Intihar VM, Tuovinen OH, Puhakka JA (2012b) Growth of Dunaliella tertiolecta and associated bacteria in photobioreactors. J Ind Microbiol Biot 39:1357–1365

    Article  CAS  Google Scholar 

  • Lakaniemi A-M, Hulatt CJ, Wakeman KD, Thomas DN, Puhakka JA (2012c) Eukaryotic and prokaryotic microbial communities during microalgal biomass production. Bioresource Technol 124:387–393

    Article  CAS  Google Scholar 

  • Le Chevanton M, Garnier M, Bougaran G, Schreiber N, Lukomska E, Bérard J-B, Fouilland E, Bernard O, Cadoret J-P (2013) Screening and selection of growth-promoting bacteria for Dunaliella cultures. Algal Res 2:212–222

    Article  Google Scholar 

  • Makridis P, Alves Costa R, Dinis MT (2006) Microbial conditions and antimicrobial activity in cultures of two microalgae species, Tetraselmis chuii and Chlorella minutissima, and effect on bacterial load of enriched Artemia metanauplii. Aquaculture 255:76–81

    Article  Google Scholar 

  • Makridis P, Ferreira T, Kokou F, Tsigenopoulos CS, Divanach P (2012) Quantitative and qualitative aspects of bacterial communities associated with cultures of Chlorella minutissima. J World Aquacult Soc 43:571–578

    Article  Google Scholar 

  • Marchesi JR, Sato T, Weightman AJ, Martin TA, Fray JC, Hiom SJ, Wade WG (1998) Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA. Appl Environ Microb 64:795–799.

  • Natrah FMI, Kenmegne MM, Wiyoto W, Sorgeloos P, Bossier P, Defoirdt T (2011) Effects of micro-algae commonly used in aquaculture on acyl-homoserine lactone quorum sensing. Aquaculture 317:53–57

    Article  CAS  Google Scholar 

  • Natrah FMI, Bossier P, Sorgeloos P, Yusoff FMD, Defoirdt T (2014) Significance of microalgal–bacterial interactions for aquaculture. Rev Aquacult 6:48–61

    Article  Google Scholar 

  • Nedashkovskaya OI, Vancanneyt M, Dawyndt P, Engelbeen K, Vandemeulebroecke K, Cleenwerck I, Hoste B, Mergaert J, Tan T-L, Frolova GM, Mikhailov VV, Swings J (2005) Reclassification of [Cytophaga] marinoflava Reichenbach 1989 as Leeuwenhoekiella marinoflava gen. nov., comb. nov. and description of Leeuwenhoekiella aequorea sp. nov. Int J Syst Evol Micr 55:1033–1038

    Article  CAS  Google Scholar 

  • Nedashkovskaya OI, Vancanneyt M, Kim SB, Bae KS (2010) Reclassification of Flexibacter tractuosus (Lewin 1969) Leadbetter 1974 and ‘Microscilla sericea’ Lewin 1969 in the genus Marivirga gen. nov. as Marivirga tractuosa comb. nov. and Marivirga sericea nom. rev., comb. nov. Int J Syst Evol Micr 60:1858–1863

    Article  Google Scholar 

  • Nicolas J-L, Corre S, Cochard J-C (2004) Bacterial population association with phytoplankton cultured in a bivalve hatchery. Microbial Ecol 48:400–413

    Article  Google Scholar 

  • Oh J-I, Kim M-J, Lee J-Y, Ko I-J, Kim W, Kim SW (2011) Isolation and characterization of algicidal bacteria from Cochlodinium polykrikoides culture. Biotechnol Bioproc E 16:1124–1133

    Article  CAS  Google Scholar 

  • Otsuka S, Abe Y, Fukui R, Nishiyama M, Senoo K (2008) Presence of previously undescribed bacterial taxa in non-axenic Chlorella cultures. J Gen Appl Microbiol 54:187–193

    Article  CAS  PubMed  Google Scholar 

  • Polz MF, Cavanaugh CM (1998) Bias in template-to-product ratios in multitemplate PCR. Appl Environ Microb 64:3724–3730

    CAS  Google Scholar 

  • Ramanan R, Kim B-H, Cho D-H, Oh H-M, Kim H-S (2016) Algae–bacteria interactions: evolution, ecology and emerging applications. Biotechnol Adv 34:14–29

    Article  CAS  PubMed  Google Scholar 

  • Regunathan C, Wesley SG (2004) Control of Vibrio spp. in shrimp hatcheries using the green algae Tetraselmis suecica. Asian Fish Sci 17:147–158

    Google Scholar 

  • Riclea R, Gleitzmann J, Bruns H, Junker C, Schulz B, Dickschat JS (2012) Algicidal lactones from the marine Roseobacter clade bacterium Ruegeria pomeroyi. Beilstein J Org Chem 8:941–950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riquelme CE, Avendaño-Herrera RE (2003) Microalgae and bacteria interaction in the aquatic environment and their potential use in aquaculture. Rev Chil Hist Nat 76:725–736

    Article  Google Scholar 

  • Sapp M, Schwaderer AS, Wiltshire KH, Hoppe H-G, Gerdts G, Wichels A (2007) Species-specific bacterial communities in the phycosphere of microalgae? Microbial Ecol 53:683–699

    Article  Google Scholar 

  • Schäfer H, Abbas B, Witte H, Muyzer G (2002) Genetic diversity of ‘satellite’ bacteria present in cultures of marine diatoms. FEMS Microbiol Ecol 42:25–35

    PubMed  Google Scholar 

  • Seyedsayamdost MR, Case RJ, Kolter R, Clardy J (2011) The Jekyll-and-Hyde chemistry of Phaeobacter gallaeciensis. Nat Chem 3:331–335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharifah EN, Eguchi M (2011) The phytoplankton Nannochloropsis oculata enhances the ability of Roseobacter clade bacteria to inhibit the growth of fish pathogen Vibrio anguillarum. PLoS One 6:e26756

  • Sison-Magnus MP, Jiang S, Tran KN, Kudela RM (2014) Host-specific adaptation governs the interaction of the marine diatom, Pseudo-nitzschia and their microbiota. ISME J 8:63–76

    Article  Google Scholar 

  • Su J, Yang X, Zhou Y, Zheng T (2011) Marine bacteria antagonistic to the harmful algal bloom species Alexandrium tamarense (Dinophyceae). Biol Control 56:132–138

    Article  Google Scholar 

  • Sule P, Belas R (2013) A novel inducer of Roseobacter motility is also a disruptor of algal symbiosis. J Bacteriol 195:637–646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki T, Muroga Y, Takahama M, Nishimura Y (1999) Roseivivax halodurans gen. nov., sp. nov and Roseivivax halotolerans sp. nov, aerobic bacteriochlorophyll-containing bacteria isolated from a saline lake. Int J Syst Bacteriol 49:629–634

  • Tatti E, Decorosi F, Viti C, Giovannetti L (2012) Despite long-term compost amendment seasonal changes are main drivers of soil fungal and bacterial population dynamics in a Tuscan vineyard. Geomicrobiol J 29:506–519

    Article  Google Scholar 

  • Teplitski M, Chen H, Rajamani S, Gao M, Merighi M, Sayre RT, Robinson JB, Rolfe BG, Bauer WD (2004) Chlamydomonas reinhardtii secretes compounds that mimic bacterial signals and interfere with quorum sensing regulation in bacteria. Plant Physiol 134:137–146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thornton DCO (2014) Dissolved organic matter (DOM) release by phytoplankton in the contemporary and future ocean. Eur J Phycol 49:20–46

    Article  CAS  Google Scholar 

  • Tosteson TR, Ballantine DL, Tosteson CG, Hansley V, Bardales AT (1989) Associated bacterial flora, growth, and toxicity of cultured benthic dinoflagellates Ostreopsis lenticularis and Gambierdiscus toxicus. Appl Environ Microb 55:137–141

    CAS  Google Scholar 

  • Tredici MR (2004) Mass production of microalgae: photobioreactors. In: Richmond A (ed) Handbook of microalgal culture: biotechnology and applied phycology. Blackwell Science, Oxford, pp 178–214

    Google Scholar 

  • Tredici MR, Rodolfi L (2004) Reactor for industrial culture of photosynthetic micro-organisms. PCT Patent WO2004/074423 [2 Sept 2004].

  • Tredici MR, Biondi N, Chini Zittelli G, Ponis E, Rodolfi L (2009) Advances in microalgal culture for aquaculture feed and other uses. In: Burnell G, Allan G (eds) New technologies in aquaculture: improving production efficiency, quality and environmental management. Woodhead Publishing, Cambridge, pp 610–676

  • Tulli F, Chini Zittelli G, Giorgi G, Poli BM, Tibaldi E, Tredici MR (2012) Effect of the inclusion of dried Tetraselmis suecica on growth, feed utilization, and fillet composition of European sea bass juveniles fed organic diets. J Aquat Food Prod Tech 21:188–197

    Article  Google Scholar 

  • Yao C, Ai J, Cao X, Xue S, Zhang W (2012) Enhancing starch production of a marine green microalga Tetraselmis subcordiformis through nutrient limitation. Bioresour Technol 118:438–444

  • Yoon J, Yasumoto-Hirose M, Matsuo Y, Nozawa M, Matsuda S, Kasai H, Yokota A (2007) Pelagicoccus mobilis gen. nov., sp. nov., Pelagicoccus albus sp. nov. and Pelagicoccus litoralis sp. nov., three novel members of subdivision 4 within the phylum ‘Verrucomicrobia’, isolated from seawater by in situ cultivation. Int J Syst Evol Micr 57:1377–1385

    Article  Google Scholar 

  • Yurkov VV, Beatty JT (1998) Aerobic anoxygenic phototrophic bacteria. Microbiol Mol Biol Rev 62:695–724

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Chen Y, Fu Y, Jiao N (2014) Draft genome sequence of the novel exopolysaccharide-producing bacterium Altibacter lentus strain JLT2010 T, isolated from deep seawater of the South China Sea. Genome Announc 2:e00954–14

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Acknowledgments

The authors are indebted to Dr Graziella Chini Zittelli of the Intitute of Ecosystem Study, CNR, Sesto Fiorentino, Florence, Italy, for providing the algal culture samples from which the isolation of the bacteria was carried out.

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Correspondence to Carlo Viti.

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Natascia Biondi and Giulia Cheloni contributed equally to this work.

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Biondi, N., Cheloni, G., Tatti, E. et al. The bacterial community associated with Tetraselmis suecica outdoor mass cultures. J Appl Phycol 29, 67–78 (2017). https://doi.org/10.1007/s10811-016-0966-5

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