Assessing niche separation among coexisting Limnohabitans strains through interactions with a competitor, viruses, and a bacterivore

. 2010 Mar ; 76 (5) : 1406-16. [epub] 20091228

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid20038688

We investigated potential niche separation in two closely related (99.1% 16S rRNA gene sequence similarity) syntopic bacterial strains affiliated with the R-BT065 cluster, which represents a subgroup of the genus Limnohabitans. The two strains, designated B4 and D5, were isolated concurrently from a freshwater reservoir. Differences between the strains were examined through monitoring interactions with a bacterial competitor, Flectobacillus sp. (FL), and virus- and predator-induced mortality. Batch-type cocultures, designated B4+FL and D5+FL, were initiated with a similar biomass ratio among the strains. The proportion of each cell type present in the cocultures was monitored based on clear differences in cell sizes. Following exponential growth for 28 h, the cocultures were amended by the addition of two different concentrations of live or heat-inactivated viruses concentrated from the reservoir. Half of virus-amended treatments were inoculated immediately with an axenic flagellate predator, Poterioochromonas sp. The presence of the predator, of live viruses, and of competition between the strains significantly affected their population dynamics in the experimentally manipulated treatments. While strains B4 and FL appeared vulnerable to environmental viruses, strain D5 did not. Predator-induced mortality had the greatest impact on FL, followed by that on D5 and then B4. The virus-vulnerable B4 strain had smaller cells and lower biomass yield, but it was less subject to grazing. In contrast, the seemingly virus-resistant D5, with slightly larger grazing-vulnerable cells, was competitive with FL. Overall, our data suggest contrasting ecophysiological capabilities and partial niche separation in two coexisting Limnohabitans strains.

Erratum v

Appl Environ Microbiol. 2010 Jun;76(11):3762 PubMed

Zobrazit více v PubMed

Alonso, C., M. Zeder, C. Piccini, D. Conde, and J. Pernthaler. 2009. Ecophysiological differences of betaproteobacterial populations in two hydrochemically distinct compartments of a subtropical lagoon. Environ. Microbiol. 11:867-876. PubMed

Bettarel, Y., T. Sime-Ngando, M. Bouvy, R. Arfi, and C. Amblard. 2005. Low consumption of virus-sized particles by heterotrophic nanoflagellates in two lakes of the French Massif Central. Aquat. Microbiol. Ecol. 39:205-209.

Brussaard, C. P. 2004. Optimization of procedures for counting viruses by flow cytometry. Appl. Environ. Microbiol. 70:1506-1513. PubMed PMC

Eiler, A., and S. Bertilsson. 2004. Composition of freshwater bacterial communities associated with cyanobacterial blooms in four Swedish lakes. Environ. Microbiol. 6:1228-1243. PubMed

Fuhrman, J. A. 1999. Marine viruses and their biogeochemical and ecological effects. Nature 399:541-548. PubMed

Gasol, J. M., and P. A. Del Giorgio. 2000. Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities. Sci. Mar. 64:197-224.

Gray, N. D., D. Comaskey, I. P. Miskin, R. W. Pickup, K. Suzuki, and I. M. Head. 2004. Adaptation of sympatric Achromatium spp. to different redox conditions as a mechanism for coexistence of functionally similar sulphur bacteria. Environ. Microbiol. 6:669-677. PubMed

Hahn, M. W. 2003. Isolation of strains belonging to the cosmopolitan Polynucleobacter necessarius cluster from freshwater habitats located in three climatic zones. Appl. Environ. Microbiol. 69:5248-5254. PubMed PMC

Hahn, M. W., and M. G. Höfle. 1998. Grazing pressure by a bacterivorous flagellate reverses the relative abundance of Comamonas acidovorans PX54 and Vibrio strain CB5 in chemostat cocultures. Appl. Environ. Microbiol. 64:1910-1918. PubMed PMC

Hahn, M. W., and M. G. Höfle. 2001. Grazing of protozoa and its effect on populations of aquatic bacteria. FEMS Microbiol. Ecol. 35:113-121. PubMed

Hahn, M. W., V. Kasalický, J. Jezbera, U. Brandt, J. Jezberová, and K. Šimek. Limnohabitans curvus gen. nov., sp. nov., a planktonic bacterium isolated from a freshwater lake. Int. J. Syst. Evol. Microbiol., in press. PubMed PMC

Hahn, M. W., E. R. B. Moore, and M. G. Höfle. 1999. Bacterial filament formation, a defense mechanism against flagellate grazing, is growth rate controlled in bacteria of different phyla. Appl. Environ. Microbiol. 65:25-35. PubMed PMC

Hahn, M. W., and M. Pöckl. 2005. Ecotypes of planktonic actinobacteria with identical 16S rRNA genes adapted to thermal niches in temperate, subtropical, and tropical freshwater habitats. Appl. Environ. Microbiol. 71:766-773. PubMed PMC

Hahn, M. W., P. Stadler, Q. L. Wu, and M. Pöckl. 2004. The filtration-acclimatization method for isolation of an important fraction of the not readily cultivable bacteria. J. Microb. Methods 57:379-390. PubMed

Horňák, K., J. Jezbera, and K. Šimek. 2008. Impact of Microcystis aeruginosa and flagellates on bacterial growth and activity in a eutrophic reservoir. Aquat. Microbiol. Ecol. 52:107-117.

Hunt, D. E., L. A. David, D. Gevers, S. P. Preheim, E. J. Alm, and M. F. Polz. 2008. Resource partitioning and sympatric differentiation among closely related bacterioplankton. Science 320:1081-1085. PubMed

Jacquet, S., I. Domaizon, S. Personnic, and T. Sime-Ngando. 2007. Do small grazers influence viral-induced bacterial mortality in Lake Bourget? Fund. Appl. Limnol. 170:125-132.

Jaspers, E., and J. Overmann. 2004. Ecological significance of microdiversity: identical 16S rRNA gene sequences can be found in bacteria with highly divergent genomes and ecophysiologies. Appl. Environ. Microbiol. 70:4831-4839. PubMed PMC

Jezbera, J., K. Horňák, and K. Šimek. 2005. Food selection by bacterivorous protists: insight from the analysis of the food vacuole content by means of fluorescence in situ hybridization. FEMS Microbiol. Ecol. 52:351-363. PubMed

Johnson, Z. I., E. R. Zinser, A. Coe, N. P. McNulty, E. M. S. Woodward, and S. W. Chisholm. 2006. Niche partitioning among Prochlorococcus ecotypes along ocean-scale environmental gradients. Science 311:1737-1740. PubMed

Lindström, E. S., M. P. Kamst-Van Agterveld, and G. Zwart. 2005. Distribution of typical freshwater bacterial groups is associated with pH, temperature, and lake water retention time. Appl. Environ. Microbiol. 71:8201-8206. PubMed PMC

Middelboe, M., Å. Hagström, N. Blackburn, B. Sinn, U. Fisher, N. H. Borch, J. Pinhassi, K. Simu, and M. G. Lorenz. 2001. Effects of bacteriophages on the population dynamics of four strains of pelagic marine bacteria. Microb. Ecol. 42:395-406. PubMed

Middelboe, M., N. O. G. Jørgensen, and N. Kroer. 1996. Effects of viruses on nutrient turnover and growth efficiency of noninfected marine bacterioplankton. Appl. Environ. Microbiol. 62:1991-1997. PubMed PMC

Middelboe, M., L. Riemann, G. L. Steward, V. Hansen, and O. Nybroe. 2003. Virus-induced transfer of organic carbon between marine bacteria in a model community. Aquat. Microb. Ecol. 33:1-10.

Miki, T., and S. Jacquet. 2008. Complex interactions in the microbial world: under-explored key links between viruses, bacteria and protozoan grazers in aquatic environments. Aquat. Microb. Ecol. 51:195-208.

Newton, R. J., S. E. Jones, M. R. Helmus, and K. D. McMahon. 2007. Phylogenetic ecology of the freshwater Actinobacteria acI lineage. Appl. Environ. Microbiol. 73:7169-7176. PubMed PMC

Noble, R. T., M. Middelboe, and J. A. Fuhrman. 1999. The effects of viral enrichment on the mortality and growth of heterotrophic bacterioplankton. Aquat. Microb. Ecol. 18:1-13.

Peréz, M. T., and R. Sommaruga. 2006. Differential effect of algal- and soil-derived dissolved organic matter on alpine lake bacterial community composition and activity. Limnol. Oceanogr. 51:2527-2537.

Pérez, M. T., and R. Sommaruga. 2007. Interactive effects of solar radiation and dissolved organic matter on bacterial activity and community structure. Environ. Microbiol. 9:2200-2210. PubMed PMC

Pernthaler, A., J. Pernthaler, and R. Amann. 2002. Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria. Appl. Environ. Microbiol. 68:3094-3101. PubMed PMC

Pernthaler, J. 2005. Predation on prokaryotes in the water column and its ecological implications. Nat. Rev. Microbiol. 3:537-546. PubMed

Posch, T., J. Pernthaler, A. Alfreider, and A. Psenner. 1997. Cell-specific respiratory activity of aquatic bacteria studied with the tetrazolium reduction method, Cyto-Clear slides, and image analysis. Appl. Environ. Microbiol. 63:867-873. PubMed PMC

Pradeep Ram, A. S., and T. Sime-Ngando. 2008. Functional responses of prokaryotes and viruses to grazer effects and nutrient additions in freshwater microcosms. ISME J. 2:498-509. PubMed

Salcher, M. M., J. Pernthaler, M. Zeder, R. Psenner, and T. Posch. 2008. Spatio-temporal niche separation of planktonic Betaproteobacteria in an oligo-mesotrophic lake. Environ. Microbiol. 10:2074-2086. PubMed

Schauer, M., J. Jiang, and M. W. Hahn. 2006. Recurrent seasonal variations in abundance and composition of filamentous SOL cluster bacteria (Saprospiraceae, Bacteroidetes) in oligomesotrophic Lake Mondsee (Austria). Appl. Environ. Microbiol. 72:4704-4712. PubMed PMC

Sekar, R., A. Pernthaler, J. Pernthaler, F. Warnecke, T. Posch, and R. Amann. 2003. An improved protocol for quantification of freshwater Actinobacteria by fluorescence in situ hybridization. Appl. Environ. Microbiol. 69:2928-2935. PubMed PMC

Šimek, K., K. Horňák, J. Jezbera, M. Mašín, J. Nedoma, J. M. Gasol, and M. Schauer. 2005. Influence of top-down and bottom-up manipulation on the R-BT065 subcluster of beta-proteobacteria, an abundant group in bacterioplankton of a freshwater reservoir. Appl. Environ. Microbiol. 71:2381-2390. PubMed PMC

Šimek, K., K. Horňák, J. Jezbera, J. Nedoma, J. Vrba, V. Straškrabová, M. Macek, J. R. Dolan, and M. W. Hahn. 2006. Maximum growth rates and possible life strategies of different bacterioplankton groups in relation to phosphorus availability in a freshwater reservoir. Environ. Microbiol. 8:1613-1624. PubMed

Šimek, K., V. Kasalický, J. Jezbera, J. Jezberová, J. Hejzlar, and M. W. Hahn. 2010. Broad habitat range of the phylogenetically narrow R-BT065 cluster, representing a core group of the betaproteobacterial genus Limnohabitans. Appl. Environ. Microbiol. 76:631-639. PubMed PMC

Šimek, K., P. Kojecká, J. Nedoma, P. Hartman, J. Vrba, and J. Dolan. 1999. Shifts in bacterial community composition associated with different microzooplankton size fractions in a eutrophic reservoir. Limnol. Oceanogr. 44:1634-1644.

Šimek, K., J. Pernthaler, M. G. Weinbauer, K. Horňák, J. R. Dolan, J. Nedoma, M. Mašín, and R. Amann. 2001. Changes in bacterial community composition, dynamics, and viral mortality rates associated with enhanced flagellate grazing in a mesoeutrophic reservoir. Appl. Environ. Microbiol. 67:2723-2733. PubMed PMC

Šimek, K., M. G. Weinbauer, K. Horňák, J. Jezbera, J. Nedoma, and J. Dolan. 2007. Grazer and virus-induced mortality of bacterioplankton accelerates development of Flectobacillus populations in a freshwater community. Environ. Microbiol. 9:789-800. PubMed

Sime-Ngando, T., and A. S. Pradeep Ram. 2005. Grazer effects on prokaryotes and viruses in a freshwater microcosm experiment. Aquat. Microb. Ecol. 41:115-124.

Suttle, C. A. 1993. Enumeration and isolation of viruses, p. 121-134. In P. F. Kemp, B. F. Sherr, E. B. Sherr, and J. J. Cole (ed.), Handbook of methods in aquatic microbial ecology. Lewis Publishers, Boca Raton, FL.

Suttle, C. A. 2007. Marine viruses—major players in global ecosystem. Nat. Rev. Microbiol. 5:801-812. PubMed

Thingstad, T. F., and R. Lignell. 1997. Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquat. Microb. Ecol. 13:19-27.

Thingstad, F., L. Øvreas, J. K. Egge, T. Løvdal, and M. Heldal. 2005. Use of nonlimiting substrates to increase size; a generic strategy to simultaneously optimize uptake and minimize predation in pelagic osmotrophs? Ecol. Lett. 8:675-682.

Weinbauer, M. 2004. Ecology of prokaryotic viruses. FEMS Microbiol. Rev. 28:127-181. PubMed

Weinbauer, M., K. Horňák, J. Jezbera, J. Nedoma, J. Dolan, and K. Šimek. 2007. Synergistic and antagonistic effects of viral lysis and protistan grazing on bacterial biomass, production and diversity. Environ. Microbiol. 9:777-788. PubMed

Zwart, G., B. C. Crump, M. Agterveld, F. Hagen, and S. K. Han. 2002. Typical freshwater bacteria: an analysis of available 16S rRNA gene sequences from plankton of lakes and rivers. Aquat. Microb. Ecol. 28:141-155.

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

The Limnohabitans Genus Harbors Generalistic and Opportunistic Subtypes: Evidence from Spatiotemporal Succession in a Canyon-Shaped Reservoir

. 2017 Nov 01 ; 83 (21) : . [epub] 20171017

Patterns of Limnohabitans microdiversity across a large set of freshwater habitats as revealed by Reverse Line Blot Hybridization

. 2013 ; 8 (3) : e58527. [epub] 20130312

The diversity of the Limnohabitans genus, an important group of freshwater bacterioplankton, by characterization of 35 isolated strains

. 2013 ; 8 (3) : e58209. [epub] 20130307

Every coin has a back side: invasion by Limnohabitans planktonicus promotes the maintenance of species diversity in bacterial communities

. 2012 ; 7 (12) : e51576. [epub] 20121212

Genome sequences of two freshwater betaproteobacterial isolates, Limnohabitans species strains Rim28 and Rim47, indicate their capabilities as both photoautotrophs and ammonia oxidizers

. 2012 Nov ; 194 (22) : 6302-3.

Alga-derived substrates select for distinct Betaproteobacterial lineages and contribute to niche separation in Limnohabitans strains

. 2011 Oct ; 77 (20) : 7307-15. [epub] 20110826

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace