Skip to main content
SpringerLink
Log in

Potential DMSP-degrading Roseobacter clade dominates endosymbiotic microflora of Pyrodinium bahamense var. compressum (Dinophyceae) in vitro

  • Short Communication
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Many aspects of the biology and ecology of the toxic dinoflagellate Pyrodinium bahamense var. compressum are still poorly understood. In this brief note, we present identification of its associated intracellular bacteria or endosymbionts via PCR cloning and 16s rRNA gene sequencing and their localization by confocal microscopy, a first for Pyrodinium. The most frequently observed species in the endosymbiotic microflora were from Roseobacter clade (Alphaproteobacteria, 68 %) and Gilvibacter sediminis (Flavobacteriaceae, 20 %). Roseobacter lineage, the most abundant taxa in this study, is known to be involved in dimethylsulfoniopropionate metabolism which is highly produced in dinoflagellates—a possible strong factor shaping the structure of the associated bacterial community.

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

References

  • Alavi M, Miller T, Erlandson K, Schneider R, Belas R (2001) Bacterial community associated with Pfiesteria-like dinoflagellate culture. Environ Microbiol 3:380–396

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Azanza MP, Azanza RV, Vargas VMD, Hedreyda CT (2006) Bacterial endosymbionts of Pyrodinium bahamense var. compressum. Microb Ecol 52:756–764

    Article  PubMed  Google Scholar 

  • Boden R, Kelly DP, Murrell JC, Schäfer H (2010) Oxidation of dimethylsulfide to tetrathionate by Methylophaga thiooxidans sp. nov.: a new link in the sulfur cycle. Environ Microbiol 12:2688–2699

    CAS  PubMed  Google Scholar 

  • Brettar I, Christen R, Hofle MG (2012) Analysis of bacterial core communities in the central Baltic by comparative RNA-DNA-based fingerprinting provides links to structure-function relationships. ISME J 6:195–212

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Buchan A, González JM, Moran MA (2005) An overview of the marine Roseobacter lineage. Appl Environ Microbiol 70:2560–2565

    Google Scholar 

  • Buchan A, LeCleir GR, Gulvik CA, González JM (2014) Master recyclers: features and functions of bacteria associated with phytoplankton blooms. Nat Rev Microbiol 12:686–698

    Article  CAS  PubMed  Google Scholar 

  • Chin GJWL, Teoh PL, Kumar SV, Anton A (2013) Ribosomal DNA analysis of marine microbes associated with toxin-producing Pyrodinium bahamense var. compressum (Bohm), a harmful algal bloom species. Pertan J Trop Agric Sci 36:179–188

    Google Scholar 

  • Doucette GJ (1995) Assessment of the interaction of prokaryotic cells with harmful algal species. In: Lassus P, Arzul G, Erard-Le Denn E, Gentien P, Marcaillou-Le Baut C (eds) Toxic marine phytoplankton. Lavoisier, Paris, pp 385–394

  • Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113

    Article  PubMed Central  PubMed  Google Scholar 

  • González JM, Kiene RP, Moran MA (1999) Transformation of sulfur compounds by an abundant lineage of marine bacteria in the alpha-subclass of the class Proteobacteria. Appl Environ Microbiol 65:3810–3819

    PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Green DH, Hart MC, Blackburn SI, Bolch CJS (2010) Bacterial diversity of Gymnodinium catenatum and its relationship to dinoflagellate toxicity. Aquat Microb Ecol 61:73–87

    Article  Google Scholar 

  • Hold GL, Smith EA, Rappe MS, Maas EW, Moore RB, Stroempl C, Stephen JR, Prosser JI, Birkbeck H, Gallacher S (2001) Characterization of bacterial communities associated with toxic and non-toxic dinoflagellates: Alexandrium spp. and Scrippsiella trochoidea. FEMS Microbiol Ecol 37:161–173

    Article  CAS  Google Scholar 

  • Howard EC, Sun S, Biers EJ, Moran MA (2008) Abundant and diverse bacteria involved in DMSP degradation in marine surface waters. Environ Microbiol 10:2397–2410

    Article  CAS  PubMed  Google Scholar 

  • Isenbarger TA, Finney M, Rios-Velasquez C, Handelsman J, Ruvkun G (2008) Miniprimer PCR: a new lens for viewing the microbial world. Appl Environ Microbiol 74:840–849

    Article  PubMed Central  CAS  PubMed  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 Microbiol 71:3483–3494

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Khan ST, Nakagawa Y, Harayama S (2007) Sediminibacter furfurosos gen. nov., sp. nov. and Gilvibacter sediminis gen. nov., sp. nov., novel members of the family Flavobacteriaceae. Int J Syst Evol Microbiol 57:265–269

    Article  PubMed  Google Scholar 

  • Kodama M, Doucette GK, Green DH (2006) Relationships between bacteria and harmful algae. Spinger, Berlin, pp 243–255

    Book  Google Scholar 

  • Lafay B, Ruimy R (1995) Rausch De Traubenberg C. Roseobacter algicola sp. nov., a new marine bacterium isolated from the phycosphere of the toxin-producing dinoflagellate Prorocentrum lima. Int J Syst Bacteriol 45:290–296

    Article  CAS  PubMed  Google Scholar 

  • Miller TR, Bellas R (2004) Dimethylsulfoniopropionate metabolism by Pfisteria-associated Roseobacter spp. Appl Environ Microbiol 70:3383–3391

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Onda DFL, Lluisma AO, Azanza RV (2014) Development, morphological characteristics and viability of temporary cysts of Pyrodiniumbahamense var. compressum (Dinophyceae) in vitro. Eur J Phycol 49:265–275

    Article  CAS  Google Scholar 

  • Pinhassi J, Simó R, González JM, Vila M, Alonso-Sáez L, Kiene RP, Moran MA, Pedrós-Alió C (2005) Dimethylsulfoniopropionate turnover is linked to the composition and dynamics of the bacterioplankton assemblage during a microcosm phytoplankton bloom. Appl Environ Microbiol 71:7650–7660

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ruh WW, Ahmad A, Mat Isa MN, Mahadi NM, Marasan NA, Usup G (2009) Diversity of bacteria associated with the benthic marine dinoflagellates Coolia monotis and Ostreopsis ovate from Malaysian waters. J Sci Tech Trop 5:23–33

    Google Scholar 

  • Santos MAG, Azanza RV (2012) Responses of Pyrodinium bahamense var. compressum and associated cultivable bacteria to antibiotic treatment. J Appl Phycol. doi:10.1007/s10811-011-9701-4

    Google Scholar 

  • Simó R, Archer SD, Pedrós-Alió C, Gilpin L, Stelfox-Widdicombe CE (2002) Coupled dynamics of dimethylsulfoniopropionate and dimethylsulfide cycling and the microbial food web in surface waters of the North Atlantic. Limnol Oceanogr 47:53–61

    Article  Google Scholar 

  • Sunda WD, Kieber WDJ, Kiene RP, Hunstman S (2002) An antioxidant function for DMSP and DMS in marine algae. Nature 418:317–320

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang H, Tomasch J, Jarek M, Wagner-Dӧbler IW (2014) A dual-species co-cultivation system to study the interactions between Roseobacters and dinoflagellates. Front Microbiol. doi:10.3389/fmicb.2014.00311

    Google Scholar 

  • Wright ES, Yilmaz S, Noguera DR (2011) DECIPHER, search-based approach to chimera identification for 16s rRNA sequences. Appl Environ Microbiol 78:717–725

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This study was part of the research program “Ecology and Oceanography of Harmful Algal Blooms in the Philippines (PhilHABs), Project 1: Biodiversity/Genetic Diversity of selected HAB-forming species in the Philippines and their associated bacterial communities”, funded and supported by the Department of Science and Technology (DOST) through the Philippine Council for Aquatic and Marine Research and Development (PCAMRD, now part of PCAARRD). We would also like to thank the Biotechnology and Molecular Genetics Research Laboratory at the UP-NIMBB headed by Dr. Ameurfina D. Santos for the use of the electroporator, Dr. Neda Barghi for her assistance in cloning, Emelita Eugenio for her help in maintaining the algal cultures, Dr. Mary Anne Santos for her comments on Pyrodinium biology, and Margaux Goudal for her valuable insights on DMSP regulation and metabolism.

Author information

Author notes

  1. Deo Florence L. Onda

    Present address: Takuvik/Quebec-Ocean/IBIS, Pavillon Eugene Marchand, Université Laval, Québec City, QC, G1V0A6, Canada

Authors and Affiliations

  1. The Marine Science Institute, University of the Philippines, 1101, Diliman, Quezon City, Philippines

    Deo Florence L. Onda, Rhodora V. Azanza & Arturo O. Lluisma

Authors
  1. Deo Florence L. Onda
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rhodora V. Azanza
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Arturo O. Lluisma
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Arturo O. Lluisma.

Ethics declarations

Conflict of interest

The authors express no conflict of interest in publishing this article.

Additional information

Communicated by Erko Stackebrandt.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Figure 1

Phylogenetic trees inferred from partial 16s rRNA genes sequenced in a.) forward and b.) reverse directions, together with the most related NCBI sequences using the maximum likelihood method in MEGA 5.0. Accession numbers are placed before the putative identities of the reference sequences. The tree is drawn to scale, with branch lengths in the same units as those of the evolutionary distances used to infer the phylogenetic tree (PNG 803 kb)

Supplementary material 2 (PNG 830 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Onda, D.F.L., Azanza, R.V. & Lluisma, A.O. Potential DMSP-degrading Roseobacter clade dominates endosymbiotic microflora of Pyrodinium bahamense var. compressum (Dinophyceae) in vitro. Arch Microbiol 197, 965–971 (2015). https://doi.org/10.1007/s00203-015-1133-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-015-1133-0

Keywords

Search

Navigation