Abstract
We studied the effects of predation on the cytometric and phylogenetic features of two enriched bacterial communities obtained from two cultures of marine heterotrophic nanoflagellates: Jakoba libera and a mixed culture of Cafeteria sp. and Monosiga sp. Protists were harvested by flow cytometric cell sorting and eight different treatments were prepared. Each bacterial community was incubated with and without protists, and we added two treatments with protists and the bacteria present after the sorting procedure (cosorted bacteria). The bacterial community derived from the culture of Jakoba libera had higher green fluorescence per cell (FL1) than that derived from the mixed culture of Cafeteria sp. and Monosiga sp. When the experiment began all treatments presented bacterial communities that increase in fluorescence per bacterium (FL1); after that the FL1 decreased when bacteria attained maximal concentrations; and, finally, there was a new increase in FL1 toward the end of the experiment. Cosorted bacteria of Jakoba libera had the same fluorescence as the bacterial community derived from this protist, while the bacteria derived from the mixed culture of Cafeteria sp. and Monosiga sp. was nearly twice as fluorescent than that of the parental community. All treatments presented a general decline of SSC along the incubation. Therefore, there was a small influence of protists on the cytometric signature of each bacterial community. However, each bacterial community preyed by Jakoba libera or the mixed culture of Cafeteria sp. and Monosiga sp. led to four different phylogenetic fingerprint. Besides, the final Communities were different from the fingerprint of controls without protists, and most of them diverge from the fingerprint of cosorted bacteria. Our results confirm that changes in the phylogenetic composition of marine bacterial communities may depend on the initial communities of both bacteria and protists.
Similar content being viewed by others
References
F Azam T Fenchel JG Field JS Gray LA Meyer-Reil F Thingstad (1983) ArticleTitleThe ecological role of water-column microbes in the sea Mar Ecol Prog Ser 10 257–263
J Boenigk H Arndt (2000) ArticleTitleComparative studies on the feeding behavior of two heterotrophic nanoflagellates: the filter-feeding choanoflagellate Monosiga ovata and the raptorial-feeding kinetoplastid Rhynchomonas nasuta Mar Ecol Prog Ser 22 243–249
J Boenigk H Arndt (2002) ArticleTitleBacterivory by heterotrophic flagellates: community structure and feeding strategies Antonie van Leeuwenhoek 81 465–480
J Boenigk C Matz K Jürgens H Arndt (2002) ArticleTitleFood concentration-dependent regulation of food selectivity on interception-feeding bacterivorous nanoflagellates Aquat Microb Ecol 27 195–202
TC Bouvier PA Giorgio ParticleDel (2002) ArticleTitleCompositional changes in free-living bacterial communities along a salinity gradient in two temperate estuaries Limnol Oceanogr 47 453–470
EO Casamayor R Massana S Benlloch L Øvreås B Díez V Goddard JM Gasol I Joint F Rodríguez-Valera C Pedrós-Alió (2002) ArticleTitleChanges in archaeal, bacterial and eukaryal assemblages along a salinity gradient by comparison of genetic fingerprinting methods in a multi-pond solar saltern Environ Microbiol 4 338–348
EO Casamayor C Pedrós-Alió G Muyzer R Amann (2002) ArticleTitleMicroheterogeneity in 16S rDNA-defined bacterial populations from a stratified planktonic environment is related to temporal changes and to ecological adaptations Appl Environ Microbiol 68 1706–1714
EO Casamayor H Schäfer L Bañeras C Pedrós-Alió G Muyzer (2000) ArticleTitleIdentification of and spatio-temporal differences between microbial assemblages from two neighboring sulfurous lakes: comparison by microscopy and denaturing gradient gel electrophoresis Appl Environ Microbiol 66 499–508
FJ Cynar KW Estep JM Sieburth (1985) ArticleTitleThe detection and characterization of bacteria-sized protist in “protist-free” filtrates and their potential impact on experimental marine ecology Microb Ecol 11 281–288
PA Giorgio ParticleDel G Scarborough (1995) ArticleTitleIncrease in the proportion of metabolically active bacteria along gradients of enrichment in freshwater and marine plankton: implications for estimates of bacterial growth and productions rates J Plankton Res 17 1905–1925
PA Giorgio ParticleDel JM Gasol D Vaqué PM Mura S Agustí CM Duarte (1996) ArticleTitleBacterioplankton community structure: protist control net production and the proportion of active bacteria in a coastal marine community Limnol Oceanogr 41 1169–1179
J-F Dumestre EO Casamayor R Massana C Pedrós-Alió (2002) ArticleTitleChanges in bacterial and archaeal assemblages in an equatorial river induced by the water eutrophication of Petit Saut dam reservoir (French Guiana) Aquat Microb Ecol 26 209–221
T Fenchel (1982) ArticleTitleEcology of heterotrophic microflagellates. IV. Quantitative occurence and importance as bacterial consumers Mar Ecol Prog Ser 9 35–42
JA Fuhrman (1999) ArticleTitleMarine viruses and their biogeochemical and ecological effects Nature 399 541–548
JM Gasol PA Giorgio ParticleDel (2000) ArticleTitleUsing flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities Sci Mar 64 197–224
FO Glökner BM Fuchs R Amann (1999) ArticleTitleBacterioplankton compositions of lakes and oceans: a first comparison based on fluorescene in situ hybridization Appl Environ Microbiol 65 3721–3726
JM González EB Sherr BF Sherr (1993) ArticleTitleDifferential feeding by marine flagellates on growing versus starving, and on motile versus nonmotile, bacterial prey Mar Ecol Prog Ser 102 257–267
MW Hahn MG Höfle (1998) ArticleTitleGrazing pressure by a bacterivorous flagellate reverses the relative abundance of Comamonas acidovorans PX 54 and a Vibrio strain CB5 in chemostat cocultures Appl Environ Microbiol 64 1910–1918
MW Hahn MG Höfle (2001) ArticleTitleGrazing of protozoa and its effect on populations of aquatic bacteria FEMS Microb Ecol 35 113–121
MW Hahn ERB Moore MG Höfle (1999) ArticleTitleBacterial filament formation, a defense mechanism against flagellate grazing, is growth rate controlled in bacteria of different phyla Appl Environ Microbiol 65 25–35
MW Hahn ERB Moore MG Höfle (2000) ArticleTitleRole of microcolony formation in the protistan grazing defense of the aquatic bacterium Pseudomonas sp MWH1. Microb Ecol 39 175–185
MG Höfle H Haas K Dominik (1999) ArticleTitleSeasonal dynamics of bacterioplancton community structure in an eutrophic lake as determined by 5s rRNA analysis Appl Environ Microbiol 65 3164–3174
K Jürgens H Güde (1994) ArticleTitleThe potential importance of grazing-resistant bacteria in planktonic systems Mar Ecol Prog Ser 112 169–188
K Jürgens C Matz (2002) ArticleTitlePredation as a shaping force for the phenotypic and genotypic composition of planktonic bacteria Ant van Leeuwen 81 413–434
K Jürgens JM Gasol D Vaque (2000) ArticleTitleBacteria–flagellate coupling in microcosms experiments in the Central Atlantic J Exp Mar Biol Ecol 245 127–147
DL Kirchman L Yu BM Fuchs R Amann (2001) ArticleTitleStructure of bacterial communities in aquatic systems as revealed by filter PCR Aquat Microb Ecol 26 13–22
S Langenheder K Jürgens (2001) ArticleTitleRegulation of bacterial biomass and community structure by metazoan and protozoan predation Limnol Oceanogr 46 121–134
P Lebaron N Parthuisot P Catala (1998) ArticleTitleComparison blue nucleic acid dyes for flow cytometric enumeration of bacteria in aquatic systems Appl Environ Microbiol 64 1725–1730
P Lebaron P Servais H Agogué C Courties F Joux (2001) ArticleTitleDoes the high nucleic acid content of individual bacterial cells allow us to discriminate between active cells and inactive cells in aquatic systems? Appl Environ Microbiol 67 1775–1782
P Lebaron P Servais A-C Baudoux M Bourrain C Courties N Parthuisot (2002) ArticleTitleVariations of bacterial-specific activity with cell size and nucleic acid content assessed by flow cytometry Aquat Microb Ecol 28 131–140
P Lebaron P Servais M Troussellier C Courties J Vives-Rego G Muyzer L Bernard T Guindulain H Schaefer E Stackebrandt (1999) ArticleTitleChanges in bacterial community structure in seawater mesocosms differing in their nutrient status Aquat Microb Ecol 19 255–267
D Marie F Partensky S Jacket D Vaulot (1997) ArticleTitleEnumeration and cell cycle analysis of natural populations of marine picoplankton by flow cytometry using the nucleic acid strain SYBR Green I Appl Environ Microbiol 63 186–193
R Massana K Jürgens (2003) ArticleTitleComposition and population dynamics of planktonic bacteria and bacterivorous flagellates in seawater chemostat cultures Aquat Microb Ecol 32 11–22
R Massana L Guillou B Díez C Pedrós-Alió (2002) ArticleTitleUnveiling the organisms behind novel eukaryotic ribosomal DNA sequences from the ocean Appl Environ Microbiol 68 4554–4558
R Massana C Pedrós-Alió EO Casamayor JM Gasol (2001) ArticleTitleChanges in marine bacterioplankton phylogenetic composition during incubations designed to measure biogeochemically significant parameters Limnol Oceanogr 46 1181–1188
D Moreira P López-Garcia (2002) ArticleTitleThe molecular ecology of microbial eukaryotes unveils a hidden world Trends Microbiol 10 31–38
RT Noble JA Fuhrman (1998) ArticleTitleUse of SYBR Green I for rapid epifluorescence counts of marine viruses and bacteria Aquat Microb Ecol 14 113–118
DJ Patterson (1990) ArticleTitleJakoba libera (Ruinen, 1938), a heterotrophic flagellate from deep oceanic sediments Mar Biol Assoc UK 70 381–393
J Pernthaler T Posch K Simek J Vrba R Amann R Psenner (1997) ArticleTitleContrasting bacterial strategies to coexist with a flagellate predator in an experimental microbial assemblage Appl Environ Microbiol 63 596–601
J Pernthaler T Posch K Simek J Vrba A Pernthaler FO Gloeckner U Nuebel R Psenner R Amann (2001) ArticleTitlePredator-specific enrichment of actinobacteria from a cosmopolitan freshwater clade in mixed continuous culture Appl Environ Microbiol 67 2145–2155
LR Pomeroy WJ Wiebe (2001) ArticleTitleTemperature and substrates as interactive limiting factors for marine heterotrophic bacteria Aquat Microb Ecol 23 187–204
KG Porter YS Feig (1980) ArticleTitleThe use of DAPI for identifying and counting aquatic microflora Limnol Oceanogr 25 943–948
R Rønn AE McCaig BS Griffiths JI Prosser (2002) ArticleTitleImpact of protozoan grazing on bacterial community structure in soil microcosms Appl Environ Microbiol 68 6094–6105
JM Rose DA Caron ME Sieracki N Poulton (2004) ArticleTitleCounting heterotrophic nanoplanktonic protists in cultures and aquatic communities by flow cytometry Aquat Microb Ecol 34 263–277
H Schäfer B Abbas H Witte G Muyzer (2002) ArticleTitleGenetic diversity of “satellite” bacteria present in cultures of marine diatoms FEMS Microb Ecol 42 25–35
P Servais EO Casamayor C Courties P Catala N Parthuisot P Lebaron (2003) ArticleTitleActivity and diversity of bacterial cells with high and low nucleic acid content Aquat Microb Ecol 33 41–51
P Servais C Courties P Lebaron M Troussellier (1999) ArticleTitleCoupling bacterial activity measurements with cell sorting by flow cytometry Microb Ecol 35 171–179
E Sherr B Sherr (1988) ArticleTitleRole of microbes in pelagic food webs: a revised concept Limnol Oceanogr 33 1225–1227
E Sherr B Sherr (2002) ArticleTitleSignificance of predation by protists in aquatic microbial food webs Ant van Leeuwen 81 293–308
EB Sherr F Rassoulzadegan BF Sherr (1989) ArticleTitleBacterivory by pelagic choreotrichous ciliates in coastal waters of the NW Mediterranean Sea Mar Ecol Prog Ser 55 235–240
S Shikano LS Luckinbill Y Kurihara (1990) ArticleTitleChanges of traits in a bacterial population associated with protozoal predation Microb Ecol 20 75–84
K Simek J Pernthaler MG Weinbauer K Hornak JR Dolan J Nedoma M Masin R Amann (2001) ArticleTitleChanges in bacterial community composition and dynamics and viral mortality rates associated with enhanced flagellate grazing in a mesoeutrophic reservoir Appl Environ Microbiol 67 2723–2733
K Simek J Vrba J Pernthaler T Posch P Hartman J Nedoma R Psenner (1997) ArticleTitleMorphological and compositional shifts in an experimental bacterial community influenced by protists with contrasting feeding modes Appl Environ Microbiol 63 587–595
MT Suzuki (1999) ArticleTitleEffect of protistan bacterivory on coastal bacterioplankton diversity Aquat Microb Ecol 20 261–272
MT Suzuki SJ Giovannoni (1996) ArticleTitleBias caused by template annealing in the amplification of mixtures of 16 rRNA genes by PCR Appl Environ Microbiol 62 625–630
F Thingstad R Lignell (1997) ArticleTitleA theoretical approach to the question of how trophic interactions control carbon demand, growth rate, abundance, and diversity Aquat Microb Ecol 13 19–27
TF Thingstad (2000) ArticleTitleElements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems Limnol Oceanogr 45 1320–1328
EJ Hannen ParticleVan M Veninga J Bloem HJ Gons HJ Laanbroek (1999) ArticleTitleGenetic changes in the bacterial community structure associated with protistan grazing Arch Hydrobiol 145 25–38
D Vaqué EO Casamayor JM Gasol (2001) ArticleTitleDynamics of whole community bacterial production and grazing losses in seawater incubations as related to the changes in the proportions of bacteria with different DNA content Aquat Microb Ecol 25 163–177
JH Vosjan GJ Noort Particlevan (1998) ArticleTitleEnumerating nucleoid-visible marine bacterioplankton: bacterial abundance determined after storage of formalin-fixed samples agrees with isopropanol rising method Aquat Microb Ecol 14 149–154
Acknowledgments
This research was funded by the EU project AIRWIN (EVK3-CT2000-00030). E.V.-D. was supported by PF0036895749 (MCYT) and is currently supported by RED 2002–2003 (AGAUR), and EOC is currently supported by the “Ramón y Cajal” program (MCYT). Paul Del Giorgio and Eva Sintes offered helpful improvements. Paul Del Giorgio kindly provided Jakoba libera and Lysotracker Green, while Cristine Dupuy provided the culture of Uronema marinum. J.M. Fortuño helped with the scanning microscopy preparations, and D.J. Patterson and A.P. Mylnikok determined the genus of mixed nanoflagellates. Finally, we especially acknowledge the staff of Horn Point (University of Maryland) and Aragó Laboratories (University of Paris VI, France), and Sandrine Lacroix, Lucía, and Rocío.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Vázquez-Domínguez, E., Casamayor, E., Català, P. et al. Different Marine Heterotrophic Nanoflagellates Affect Differentially the Composition of Enriched Bacterial Communities. Microb Ecol 49, 474–485 (2005). https://doi.org/10.1007/s00248-004-0035-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-004-0035-5