AME 61:105-117 (2010)  -  DOI: https://doi.org/10.3354/ame01440

Putative N2-fixing heterotrophic bacteria associated with dinoflagellate–Cyanobacteria consortia in the low-nitrogen Indian Ocean

Hanna Farnelid1, Woraporn Tarangkoon2,3, Gert Hansen4, Per Juel Hansen2, Lasse Riemann1,5,*

1Department of Natural Sciences, Linnaeus University, 39182 Kalmar, Sweden
2Section for Marine Biology, Strandpromenaden 5, 3000 Helsingør, Denmark
3Faculty of Science and Fisheries Technology, Rajamangala University of Technology Srivijaya, 92150 Trang, Thailand
4Department of Phycology, Ø. Farimagsgade 2D, 1353, Copenhagen, Denmark
5Present address: Section for Marine Biology, Strandpromenaden 5, 3000 Helsingør, Denmark
*Corresponding author. E-mail:

ABSTRACT: Heterotrophic dinoflagellates bearing unicellular cyanobacterial symbionts are common within the order Dinophysiales. However, the ecological role of these symbionts is unclear. Due to the occurrence of such consortia in oceanic waters characterized by low nitrogen concentrations, we hypothesized that the symbionts fix gaseous nitrogen (N2). Individual heterotrophic dinoflagellates containing cyanobacterial symbionts were isolated from the open Indian Ocean and off Western Australia, and characterized using light microscopy, transmission electron microscopy (TEM), and nitrogenase (nifH) gene amplification, cloning, and sequencing. Cyanobacteria, heterotrophic bacteria and eukaryotic algae were recognized as symbionts of the heterotrophic dinoflagellates. nifH gene sequences were obtained from 23 of 37 (62%) specimens of dinoflagellates (Ornithocercus spp. and Amphisolenia spp.). Interestingly, only 2 specimens contained cyanobacterial nifH sequences, while 21 specimens contained nifH genes related to heterotrophic bacteria. Of the 137 nifH sequences obtained 68% were most similar to Alpha-, Beta-, and Gammaproteobacteria, 8% clustered with anaerobic bacteria, and 5% were related to second alternative nitrogenases (anfH). Twelve sequences from 5 host cells formed a discrete cluster which may represent a not yet classified nifH cluster. Eight dinoflagellates contained only 1 type of nifH sequence (>99% sequence identity) but overall the putative N2-fixing symbionts did not appear host specific and mixed assemblages were often found in single host cells. This study provides the first insights into the nifH diversity of dinoflagellate symbionts and suggests a symbiotic co-existence of non-diazotrophic cyanobacteria and N2-fixing heterotrophic bacteria in heterotrophic dinoflagellates.


KEY WORDS: Symbionts · Nitrogen fixation · Nitrogenase · Heterotrophic bacteria · Ornithocercus · Amphisolenia · Histioneis · Dinoflagellates · Indian Ocean · Galathea 3


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Cite this article as: Farnelid H, Tarangkoon W, Hansen G, Hansen PJ, Riemann L (2010) Putative N2-fixing heterotrophic bacteria associated with dinoflagellate–Cyanobacteria consortia in the low-nitrogen Indian Ocean. Aquat Microb Ecol 61:105-117. https://doi.org/10.3354/ame01440

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