Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Importance of free-living and particle-associated bacteria for the growth of the harmful dinoflagellate Prorocentrum minimum: evidence in culture stages

Bum Soo Park A C , Ruoyu Guo A , Weol-Ae Lim B and Jang-Seu Ki A D
+ Author Affiliations
- Author Affiliations

A Department of Biotechnology, Sangmyung University, Seoul 03016, South Korea.

B Ocean Climate and Ecology Research Division, National Institute of Fisheries Science, Busan 46083, South Korea.

C Present address: Marine Science Institute, University of Texas at Austin, Port Aransas, TX 78373, USA.

D Corresponding author. Email: kijs@smu.ac.kr

Marine and Freshwater Research 69(2) 290-299 https://doi.org/10.1071/MF17102
Submitted: 14 April 2017  Accepted: 8 August 2017   Published: 3 October 2017

Abstract

The marine dinoflagellate Prorocentrum minimum is the cause of harmful algal blooms and may grow in association with co-occurring bacteria as ectosymbiotic, endosymbiotic and free-living forms. In the present study we investigated the bacterial community composition of both free-living bacteria (FLB) and particle-associated bacteria (PAB) in the lag, exponential and stationary growth stages of P. minimum using pyrosequencing. Metagenomics, hierarchical cluster and non-metric multidimensional scaling analyses revealed that FLB and PAB had significantly different bacterial community compositions. The PAB community had greater taxonomic richness and diversity than the FLB community. In addition, the shared bacteria identified were clearly dominant in both the FLB (≥98.2%) and PAB (≥89.9%) communities. Among shared bacteria, the genera Seohaeicola (P. minimum operational taxonomic unit (OTU) #1) and Roseovarius (P. minimum OTU #6), belonging to the Roseobacter clade, were predominant in FLB (42–57%) and PAB (11–14%) communities respectively. In the PAB community, the Marinobacter clade (P. minimum OTU #13 and #15) was also a dominant taxon. Interestingly, in response to the growth of P. minimum, the proportion of the Roseobacter clade increased gradually, whereas the genus Marinobacter decreased in both the FLB and PAB communities. These results suggest that Roseobacter and Marinobacter clades are intimately associated with host dinoflagellate.

Additional keywords: associated bacterial community composition, Roseobacter.


References

Amaro, A. M., Fuentes, M. S., Ogalde, S. R., Venegas, J. A., and Suárez-Isla, B. A. (2005). Identification and characterization of potentially algal‐lytic marine bacteria strongly associated with the toxic dinoflagellate Alexandrium catenella. The Journal of Eukaryotic Microbiology 52, 191–200.
Identification and characterization of potentially algal‐lytic marine bacteria strongly associated with the toxic dinoflagellate Alexandrium catenella.Crossref | GoogleScholarGoogle Scholar |

Amin, S. A., Green, D. H., Hart, M. C., Küpper, F. C., Sunda, W. G., and Carrano, C. J. (2009). Photolysis of iron–siderophore chelates promotes bacterial–algal mutualism. Proceedings of the National Academy of Sciences of the United States of America 106, 17071–17076.
Photolysis of iron–siderophore chelates promotes bacterial–algal mutualism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlaksL%2FP&md5=2ef2b2fc2d46f22226fd543cb2ba7e39CAS |

Amin, S. A., Hmelo, L. R., van Tol, H. M., Durham, B. P., Carlson, L. T., Heal, K. R., Morales, R. L., Berthiaume, C. T., Parker, M. S., Djunaedi, B., Ingalls, A. E., Parsek, M. R., Moran, M. A., and Armbrust, E. V. (2015). Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 522, 98–101.
Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtFeitLrN&md5=2fd777b720067279026ede3230320e0aCAS |

Andersson, A. F., Lindberg, M., Lindberg, M., Jakobsson, H., Bäckhed, F., Nyrén, P., and Engstrand, L. (2008). Comparative analysis of human gut microbiota by barcoded pyrosequencing. PLoS One 3, e2836.
Comparative analysis of human gut microbiota by barcoded pyrosequencing.Crossref | GoogleScholarGoogle Scholar |

Ashen, J. B., Cohen, J. D., and Goff, L. J. (1999). GC-SIM-MS detection and quantification of free indole-3-acetic acid bacterial galls on the marine alga Prionitis lanceolata (Rhodophyta). Journal of Phycology 35, 493–500.
GC-SIM-MS detection and quantification of free indole-3-acetic acid bacterial galls on the marine alga Prionitis lanceolata (Rhodophyta).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXksl2hsr4%3D&md5=95b4091a2c93a89c872b042e33dc9742CAS |

Azam, F., and Malfatti, F. (2007). Microbial structuring of marine ecosystems. Nature 10, 782–791.

Bagatini, I. L., Eiler, A., Bertilsson, S., Klaveness, D., Tessarolli, L. P., and Vieira, A. A. H. (2014). Host-specificity and dynamics in bacterial communities associated with bloom-forming freshwater phytoplankton. PLoS One 9, e85950.
Host-specificity and dynamics in bacterial communities associated with bloom-forming freshwater phytoplankton.Crossref | GoogleScholarGoogle Scholar |

Bates, S. S., Gaudet, J., Kaxzmarska, I., and Ehrman, J. M. (2004). Interaction between bacteria and the domoic-acid-producing diatom Pseudo-nitzschia multiseries (Hasle) Hasle; can bacteria produce domoic acid autonomously? Harmful Algae 3, 11–20.
Interaction between bacteria and the domoic-acid-producing diatom Pseudo-nitzschia multiseries (Hasle) Hasle; can bacteria produce domoic acid autonomously?Crossref | GoogleScholarGoogle Scholar |

Behrenfeld, M. J., Boss, E., Siegel, D. A., and Shea, D. M. (2005). Carbon-based ocean productivity and phytoplankton physiology from space. Global Biogeochemical Cycles 19, GB1006.
Carbon-based ocean productivity and phytoplankton physiology from space.Crossref | GoogleScholarGoogle Scholar |

Bjørrisen, P. K. (1988). Phytoplankton exudation of organic matter: why do healthy cells do it? Limnology and Oceanography 33, 151–154.
Phytoplankton exudation of organic matter: why do healthy cells do it?Crossref | GoogleScholarGoogle Scholar |

Buchan, A., Gonzalez, J. M., and Moran, M. A. (2005). Overview of the marine Roseobacter lineage. Applied and Environmental Microbiology 71, 5665–5677.
Overview of the marine Roseobacter lineage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFajtbzM&md5=b218b4d58b25ca99dd6653e763cdd13fCAS |

Buchan, A., LeCleir, G. R., Gulvik, C. A., and González, J. M. (2014). Master recycler: features and functions of bacteria associated with phytoplankton blooms. Nature Reviews. Microbiology 12, 686–698.
Master recycler: features and functions of bacteria associated with phytoplankton blooms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlOlu7%2FF&md5=ad5784957900ec3d8f347a14339381ecCAS |

Crump, B. C., Armbrust, E. V., and Baross, J. A. (1999). Phylogenetic analysis of particle-attached and free-living bacterial communities in the Columbia River, its estuary, and the adjacent coastal ocean. Applied and Environmental Microbiology 65, 3192–3204.
| 1:CAS:528:DyaK1MXktlemu78%3D&md5=66bc6f203a6f983ebb228001a4ec7f24CAS |

Cruz-López, R., and Maske, H. (2016). The vitamin B1 and B12 required by the marine dinoflagellate Lingulodinium polyedrum can be provided by its associated bacterial community in culture. Frontiers in Microbiology 7, 1–13.
The vitamin B1 and B12 required by the marine dinoflagellate Lingulodinium polyedrum can be provided by its associated bacterial community in culture.Crossref | GoogleScholarGoogle Scholar |

DeLong, E. F., Franks, D. G., and Alldredge, A. L. (1993). Phylogenetic diversity of aggregate-attached vs free-living marine bacterial assemblages. Limnology and Oceanography 38, 924–934.
Phylogenetic diversity of aggregate-attached vs free-living marine bacterial assemblages.Crossref | GoogleScholarGoogle Scholar |

Dittami, S. M., Barbeyron, T., Boyen, C., Cambefort, J., Collet, G., Delage, L., Gobet, A., Groisillier, A., Leblanc, C., Michel, G., Scornet, D., Siegel, A., Tapia, J. E., and Tonon, T. (2014). Genome and metabolic network of ‘Candidatus Phaeomarinobacter ectocarpi’ Ec32, a new candidate genus of Alphaproteobacteria frequently associated with brown algae. Frontiers in Genetics 5, 241.
Genome and metabolic network of ‘Candidatus Phaeomarinobacter ectocarpi’ Ec32, a new candidate genus of Alphaproteobacteria frequently associated with brown algae.Crossref | GoogleScholarGoogle Scholar |

Gontcharova, V., Youn, E., Wolcott, R. D., Hollister, E. B., Gentry, T. J., and Dowd, S. E. (2010). Black box chimera check (B2C2): a windows-based software for batch depletion of chimeras from bacterial 16S rRNA gene datasets. The Open Microbiology Journal 4, 47–52.
Black box chimera check (B2C2): a windows-based software for batch depletion of chimeras from bacterial 16S rRNA gene datasets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVCitbrF&md5=9ea979838e91727b6b775fec9fc58dbcCAS |

González, J. M., Kiene, R. P., and Moran, M. A. (1999). Transformation of sulfur compounds by an abundant lineage of marine bacteria in the α-subclass of the Class Proteobacteria. Applied and Environmental Microbiology 65, 3810–3819.

Grossart, H. P. (1999). Interactions between marine bacteria and axenic diatoms (Cylindrotheca fusiformis, Nitzschia laevis, and Thlalassiosira weissflogii) incubated under various conditions in the lab. Aquatic Microbial Ecology 19, 1–11.
Interactions between marine bacteria and axenic diatoms (Cylindrotheca fusiformis, Nitzschia laevis, and Thlalassiosira weissflogii) incubated under various conditions in the lab.Crossref | GoogleScholarGoogle Scholar |

Grossart, H. P., Levold, F., Allgaier, M., Simon, M., and Brinkhoff, T. (2005). Marine diatom species harbour distinct bacterial communities. Environmental Microbiology 7, 860–873.
Marine diatom species harbour distinct bacterial communities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltlCqsr4%3D&md5=ac4efa887275aaf3d6674a7a2eaad2e1CAS |

Hamady, M., Walker, J. J., Harris, J. K., Gold, N. J., and Knight, R. (2008). Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex. Nature Methods 5, 235–237.
Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXisFOmtLg%3D&md5=3940aa6c895ffdca17288a6e7856317dCAS |

Hasegawa, M., Kishino, K., and Yano, T. (1985). Dating the human–ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22, 160–174.
Dating the human–ape splitting by a molecular clock of mitochondrial DNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXmtFSns7g%3D&md5=95182f724907196ec8569ba7f5e63b6fCAS |

Heil, C. A., Glibert, P. M., and Fan, C. (2005). Prorocentrum minimum (Pavillard) Schiller: a review of a harmful algal bloom species of growing worldwide importance. Harmful Algae 4, 449–470.
Prorocentrum minimum (Pavillard) Schiller: a review of a harmful algal bloom species of growing worldwide importance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXivVCmtLo%3D&md5=30916b18912bc63570ba9360ae2034eeCAS |

Hellebust, J. A. (1965). Excretion of some organic compounds by marine phytoplankton. Limnology and Oceanography 10, 192–206.
Excretion of some organic compounds by marine phytoplankton.Crossref | GoogleScholarGoogle Scholar |

Huse, S. M., Huber, J. A., Morrison, H. G., Sogin, M. L., and Welch, D. M. (2007). Accuracy and quality of massively parallel DNA pyrosequencing. Genome Biology 8, R143.
Accuracy and quality of massively parallel DNA pyrosequencing.Crossref | GoogleScholarGoogle Scholar |

Jasti, S., Sieracki, Me., Poulton, N. J., Giewat, M. W., and Rooney-Varga, J. N. (2005). Phylogenetic diversity and specificity of bacteria closely associated with Alexandrium spp. and other phytoplankton. Applied and Environmental Microbiology 71, 3483–3494.
Phylogenetic diversity and specificity of bacteria closely associated with Alexandrium spp. and other phytoplankton.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmt1ylsLY%3D&md5=5b2cf7099ac6bdd51cce3d57f9a93302CAS |

Kruskal, J. B. (1964). Multidimensional-scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika 29, 1–27.
Multidimensional-scaling by optimizing goodness of fit to a nonmetric hypothesis.Crossref | GoogleScholarGoogle Scholar |

Lane, D. J. (1991). 16S/23S rRNA sequencing. In ‘Nucleic Acid Techniques in Bacterial Systematics’. (Eds E. Stackebrandt and M. Goodfellow.) pp. 115–175. (Wiley: Chichester, UK.)

Li, W., Fu, L., Niu, B., Wu, S., and Wooley, J. (2012). Ultrafast clustering algorithms for metagenomic sequence analysis. Briefings in Bioinformatics 13, 656–668.
Ultrafast clustering algorithms for metagenomic sequence analysis.Crossref | GoogleScholarGoogle Scholar |

Magurran, A. E. (2013). ‘Measuring Biological Diversity.’ (Wiley: New York, NY, USA.)

Mayali, X., and Azam, F. (2004). Algicidal bacteria in the sea and their impact on algal blooms. The Journal of Eukaryotic Microbiology 51, 139–144.
Algicidal bacteria in the sea and their impact on algal blooms.Crossref | GoogleScholarGoogle Scholar |

Merzouk, A., Levasseur, M., Scarratt, M., Michaud, S., Lizotte, M., Rivkin, R. B., and Kiene, R. P. (2008). Bacterial DMSP metabolism during the senescence of the spring diatom bloom in the northwest Atlantic. Marine Ecology Progress Series 369, 1–11.
Bacterial DMSP metabolism during the senescence of the spring diatom bloom in the northwest Atlantic.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVOqsbvJ&md5=01d84704df845075251c3ccb7060a312CAS |

Muyzer, G., Hottenträger, S., Teske, A., and Wawer, C. (1996). Denaturing gradient gel electrophoresis of PCR-amplified 16S rDNA – a new molecular approach to analyse the genetic diversity of mixed microbial communities. In ‘Molecular Microbial Ecology Manual’. (Eds A. D. L. Akkermans, J. D. Van Elsas, and F. De Bruijn.) pp. 3.4.4/1–23. (Kluwer Academic Publishers: Dordrecht, Netherlands.)

Myklestad, S. M. (2000). Dissolved organic carbon from phytoplankton. In ‘The Handbook of Environmental Chemistry. Vol. 5D’. (Ed. P. Wangersky.) pp. 111–148. (Springer: New York, NY, USA.)

Newton, R. J., Griffin, L. E., Bowles, K. M., Meile, C., Gifford, S., Givens, C. E., Howard, E. C., King, E., Oakley, C. A., Reisch, C. R., Rinta-Kanto, J. M., Sharma, S., Sun, S., Varaljay, V., Vila-Costa, M., Westrich, J. R., and Moran, M. A. (2010). Genome characteristics of a generalist marine bacterial lineage. The ISME Journal 4, 784–798.
Genome characteristics of a generalist marine bacterial lineage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmtFCns78%3D&md5=1d158904edf8503c6b18747717607bc2CAS |

Noble, P. A., Bidle, K. D., and Fletcher, M. (1997). Natural microbial community compositions compared by a back-propagating neural network and cluster analysis of 5S rRNA. Applied and Environmental Microbiology 63, 1762–1770.
| 1:CAS:528:DyaK2sXjtFGmsL0%3D&md5=dc4ac2cad04e578dbf79bb26bf82c960CAS |

Park, B. S., Wang, P., Kim, J. H., Kim, J.-H., Gobler, C. J., and Han, M.-S. (2014). Resolving the intra-specific succession within Cochlodinium polykrikoides populations in southern Korean coastal waters via use of quantitative PCR assays. Harmful Algae 37, 133–141.
Resolving the intra-specific succession within Cochlodinium polykrikoides populations in southern Korean coastal waters via use of quantitative PCR assays.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFSqsLrP&md5=b1572313930489ba6d3eb3b815f29eb4CAS |

Park, B. S., Kim, J.-H., Kim, J. H., Gobler, C. J., Baek, S. H., and Han, M.-S. (2015). Dynamics of bacterial community structure during blooms of Cochlodinium polykrikoides (Gymnodiniales, Dinophyceae) in Korean coastal waters. Harmful Algae 48, 44–54.
Dynamics of bacterial community structure during blooms of Cochlodinium polykrikoides (Gymnodiniales, Dinophyceae) in Korean coastal waters.Crossref | GoogleScholarGoogle Scholar |

Park, B. S., Joo, J.-H., Baek, K.-D., and Han, M.-S. (2016). A mutualistic interaction between the bacterium Pseudomonas asplenii and the harmful algal species Chattonella marina (Raphidophyceae). Harmful Algae 56, 29–36.
A mutualistic interaction between the bacterium Pseudomonas asplenii and the harmful algal species Chattonella marina (Raphidophyceae).Crossref | GoogleScholarGoogle Scholar |

Parveen, B., Mary, I., Vellet, A., Ravet, V., and Debroas, D. (2013). Temporal dynamics and phylogenetic diversity of free-living and particle-associated Verrucomicrobia communities in relation to environmental variables in a mesotrophic lake. FEMS Microbiology Ecology 83, 189–201.
Temporal dynamics and phylogenetic diversity of free-living and particle-associated Verrucomicrobia communities in relation to environmental variables in a mesotrophic lake.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlemsrg%3D&md5=5a1db9e2587cf692d1176cd1668fa85eCAS |

Pinhassi, J., Sala, M. M., Havskum, H., Peters, F., Guadayol, Ò., Malits, A., and Marrasé, C. (2004). Changes in bacterioplankton composition under different phytoplankton regimens. Applied and Environmental Microbiology 70, 6753–6766.
Changes in bacterioplankton composition under different phytoplankton regimens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVSju73P&md5=f27b63684e35ced87e190defc2a25289CAS |

Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., and Glöckner, F. O. (2013). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research 41, D590–D596.
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvV2ksb%2FN&md5=92b6c092b8fe98b63386797679537dc2CAS |

Reitan, K. I., Rainuzzo, J. R., and Olsen, Y. (1994). Effect of nutrient limitation on fatty acid and lipid content of marine microalgae. Journal of Phycology 30, 972–979.
Effect of nutrient limitation on fatty acid and lipid content of marine microalgae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXkt1Chs7g%3D&md5=228e31b25381fd224338c5720d7e5b1dCAS |

Riemann, L., and Winding, A. (2001). Community dynamics of free-living and particle-associated bacterial assemblages during a freshwater phytoplankton bloom. Microbial Ecology 42, 274–285.
Community dynamics of free-living and particle-associated bacterial assemblages during a freshwater phytoplankton bloom.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XksFM%3D&md5=f667d7036c52ce5845215637686d4a43CAS |

Riemann, L., Steward, G. F., and Azam, F. (2000). Dynamics of bacterial community composition and activity during a mesocosm diatom bloom. Applied and Environmental Microbiology 66, 578–587.
Dynamics of bacterial community composition and activity during a mesocosm diatom bloom.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhtFeru7o%3D&md5=3bc05f40a7432a61a4e696f8fd6793d0CAS |

Rooney-Varga, J. N., Giewat, M. W., Savin, M. C., LeGresley, M., and Martin, J. L. (2005). Links between phytoplankton and bacterial community dynamics in a coastal marine environment. Microbial Ecology 49, 163–175.
Links between phytoplankton and bacterial community dynamics in a coastal marine environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjslyis7Y%3D&md5=4acd0d00dbc9164b1cefc58d63b28e4dCAS |

Rösel, S., and Grossart, H.-P. (2012). Contrasting dynamics in activity and community composition of free-living and particle-associated bacteria in spring. Aquatic Microbial Ecology 66, 169–181.
Contrasting dynamics in activity and community composition of free-living and particle-associated bacteria in spring.Crossref | GoogleScholarGoogle Scholar |

Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., Lesniewski, R. A., Oakley, B. B., Parks, D. H., Robinson, C. J., Sahl, J. W., Stres, B., Thallinger, G. G., Van Horn, D. J., and Weber, C. F. (2009). Introducing mothur: open-source, platformindependent, community-supported software for describing and comparingmicrobial communities. Applied and Environmental Microbiology 75, 7537–7541.
Introducing mothur: open-source, platformindependent, community-supported software for describing and comparingmicrobial communities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXis1yltw%3D%3D&md5=3b7a8e6f7325f0850fd3419272f706bcCAS |

Seyedsayamdost, M. R., Case, R. J., Kolter, R., and Clardy, J. (2011). The Jekyll-and-Hyde chemistry of Phaeobacter gallaeciensis. Nature Chemistry 3, 331–335.
The Jekyll-and-Hyde chemistry of Phaeobacter gallaeciensis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjvVKqsrk%3D&md5=e79f87c08e0756437c39beb94f9f39f7CAS |

Simon, M., Glockner, F. O., and Amann, R. (1999). Different community structure and temperature optima of heterotrophic picoplankton in various regions of the Southern Ocean. Aquatic Microbial Ecology 18, 275–284.
Different community structure and temperature optima of heterotrophic picoplankton in various regions of the Southern Ocean.Crossref | GoogleScholarGoogle Scholar |

Sison-Mangus, M. P., Jiang, S., Tran, K. N., and Kudela, R. M. (2014). Host-specific adaptation governs the interaction of the marine diatom, Pseudo-nitzschia and their microbiota. The ISME Journal 8, 63–76.
Host-specific adaptation governs the interaction of the marine diatom, Pseudo-nitzschia and their microbiota.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvFOmtLbK&md5=70fd74d5c4e3ae5a0a4368f2fe12ec2dCAS |

Stoecker, D. K., Li, A., Coats, D. W., Gustafson, D. E., and Nannen, M. K. (1997). Mixotrophy in the dinoflagellate Prorocentrum minimum. Marine Ecology Progress Series 152, 1–12.
Mixotrophy in the dinoflagellate Prorocentrum minimum.Crossref | GoogleScholarGoogle Scholar |

Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.
MEGA6: molecular evolutionary genetics analysis version 6.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVKhurzP&md5=d57c6174d530fddb3189b5d96b97096fCAS |

Tang, Y. Z., Koch, F., and Gobler, C. J. (2010). Most harmful algal bloom species are vitamin B1 and B12 auxotrophs. Proceedings of the National Academy of Sciences of the United States of America 107, 20756–20761.
Most harmful algal bloom species are vitamin B1 and B12 auxotrophs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFeit7jN&md5=754d6b10db37a114873538b53605378cCAS |

Tang, X., Li, L., Shao, K., Wang, B., Cai, X., Zhang, L., Chao, J., and Gao, G. (2015). Pyrosequencing analysis of free-living and attached bacterial communities in Meiliang Bay, Lake Taihu, a large eutrophic shallow lake in China. Canadian Journal of Microbiology 61, 22–31.
Pyrosequencing analysis of free-living and attached bacterial communities in Meiliang Bay, Lake Taihu, a large eutrophic shallow lake in China.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXkslGhtQ%3D%3D&md5=40048695612f6a0ed8c996499d80b4a8CAS |

Taylor, J. D., Cottingham, S. D., Billinge, J., and Cunliffe, M. (2014). Seasonal microbial community dynamics correlate with phytoplankton-derived polysaccharides in surface coastal waters. The ISME Journal 8, 245–248.
Seasonal microbial community dynamics correlate with phytoplankton-derived polysaccharides in surface coastal waters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvFOlt77F&md5=c2708e8d1bdff3ef657c533ab7543848CAS |

Teeling, H., Fuchs, B. M., Becher, D., Klockow, C., Gardebrecht, A., Bennke, C. M., Kassabgy, M., Huang, S., Mann, A. J., Waldmann, J., Weber, M., Klindworth, A., Otto, A., Lange, J., Bernhardt, J., Reinsch, C., Hecker, M., Peplies, J., Bockelmann, F. D., Callies, U., Gerdts, G., Wichels, A., Wiltshire, K. H., Glöckner, F. O., Schweder, T., and Amann, R. (2012). Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science 336, 608–611.
Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xmt1Gntrw%3D&md5=99738af2d2bea189dea01fa31c55ec23CAS |

Thomas, T., Gilbert, J., and Meyer, F. (2012). Metagenomics – a guide from sampling to data analysis. Microbial Informatics and Experimentation 2, 3.
Metagenomics – a guide from sampling to data analysis.Crossref | GoogleScholarGoogle Scholar |

Uribe, P., and Espejo, R. T. (2003). Effect of associated bacteria on the growth and toxicity of Alexandrium catenella. Applied and Environmental Microbiology 69, 659–662.
Effect of associated bacteria on the growth and toxicity of Alexandrium catenella.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkvVejtA%3D%3D&md5=a4f1338927c762b3d1ad387142c40908CAS |

van Rijssel, M., Janse, I., Noordkamp, D. J. B., and Gieskes, W. W. C. (2000). An inventory of factors that affect polysaccharide production by Phaeocystis globose. Journal of Sea Research 43, 297–306.
An inventory of factors that affect polysaccharide production by Phaeocystis globose.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXms1Wrur4%3D&md5=90b0c9a14b398b9c6cece8020a91d121CAS |

Wagner-Döbler, I., and Bibel, H. (2006). Environmental biology of the marine Roseobacter lineage. Annual Review of Microbiology 60, 255–280.
Environmental biology of the marine Roseobacter lineage.Crossref | GoogleScholarGoogle Scholar |

Wagner-Döbler, I., Ballhausen, B., Berger, M., Brinkhoff, T., Buchholz, I., Bunk, B., Cypionka, H., Daniel, R., Drepper, T., Gerdts, G., Hahnke, S., Han, C., Jahn, D., Kalhoefer, D., Kiss, H., Klenk, H. P., Kyrpides, N., Liebl, W., Liesegang, H., Meincke, L., Pati, A., Petersen, J., Piekarski, T., Pommerenke, C., Pradella, S., Pukall, R., Rabus, R., Stackebrandt, E., Thole, S., Thompson, L., Tielen, P., Tomasch, J., von Jan, M., Wanphrut, N., Wichels, A., Zech, H., and Simon, M. (2010). The complete genome sequence of the algal symbiont Dinoroseobacter shibae: a hitchhiker’s guide to life in the sea. The ISME Journal 4, 61–77.
The complete genome sequence of the algal symbiont Dinoroseobacter shibae: a hitchhiker’s guide to life in the sea.Crossref | GoogleScholarGoogle Scholar |

Wemheuer, B., Güllert, S., Billerbeck, S., Giebel, H. A., Voget, S., Simon, M., and Daniel, R. (2014). Impact of a phytoplankton bloom on the diversity of the active bacterial community in the southern North Sea as revealed by metatranscriptomic approaches. FEMS Microbiology Ecology 87, 378–389.
Impact of a phytoplankton bloom on the diversity of the active bacterial community in the southern North Sea as revealed by metatranscriptomic approaches.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhs1OrsLc%3D&md5=e5e241d6c4769f24b2fdd4b76f358f50CAS |

Worm, J., and Sondergaard, M. (1998). Dynamics of heterotrophic bacteria attached to Microcystis spp. (Cyanobacteria). Aquatic Microbial Ecology 14, 19–28.
Dynamics of heterotrophic bacteria attached to Microcystis spp. (Cyanobacteria).Crossref | GoogleScholarGoogle Scholar |

Zhang, R., Liu, B. Z., Lau, S. C. K., Ki, J. S., and Qian, P. Y. (2007). Particle-attached and free-living bacterial communities in a contrasting marine environment: Victoria Harbour, Hong Kong. FEMS Microbiology Ecology 61, 496–508.
Particle-attached and free-living bacterial communities in a contrasting marine environment: Victoria Harbour, Hong Kong.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVSmsLnM&md5=90f28fbe9cbfb906bf0b9e5cf9c300e4CAS |

Zhang, Q., Song, J., Yu, R., Yan, T., Wang, Y., Kong, F., and Zhou, M. (2013). Roles of mixotrophy in blooms of different dinoflagellates: implications from the growth experiment. Harmful Algae 30, 10–26.
Roles of mixotrophy in blooms of different dinoflagellates: implications from the growth experiment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVelu7rE&md5=4d0195d0effd0e486a671c3228631d03CAS |