The diversity of the Limnohabitans genus, an important group of freshwater bacterioplankton, by characterization of 35 isolated strains
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
23505469
PubMed Central
PMC3591437
DOI
10.1371/journal.pone.0058209
PII: PONE-D-12-35993
Knihovny.cz E-zdroje
- MeSH
- Betaproteobacteria klasifikace genetika růst a vývoj metabolismus MeSH
- biomasa MeSH
- ekosystém * MeSH
- fylogeneze MeSH
- genetická variace * MeSH
- molekulární sekvence - údaje MeSH
- RNA ribozomální 16S genetika MeSH
- sladká voda mikrobiologie MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- RNA ribozomální 16S MeSH
Bacteria of the genus Limnohabitans, more precisely the R-BT lineage, have a prominent role in freshwater bacterioplankton communities due to their high rates of substrate uptake and growth, growth on algal-derived substrates and high mortality rates from bacterivory. Moreover, due to their generally larger mean cell volume, compared to typical bacterioplankton cells, they contribute over-proportionally to total bacterioplankton biomass. Here we present genetic, morphological and ecophysiological properties of 35 bacterial strains affiliated with the Limnohabitans genus newly isolated from 11 non-acidic European freshwater habitats. The low genetic diversity indicated by the previous studies using the ribosomal SSU gene highly contrasted with the surprisingly rich morphologies and different patterns in substrate utilization of isolated strains. Therefore, the intergenic spacer between 16S and 23S rRNA genes was successfully tested as a fine-scale marker to delineate individual lineages and even genotypes. For further studies, we propose the division of the Limnohabitans genus into five lineages (provisionally named as LimA, LimB, LimC, LimD and LimE) and also additional sublineages within the most diversified lineage LimC. Such a delineation is supported by the morphology of isolated strains which predetermine large differences in their ecology.
PLoS One. 2013;8(9). doi:10.1371/annotation/4fe772bd-a77f-4142-92c2-256be161f263 PubMed
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Glöckner FO, Fuchs BM, Amann R (1999) Bacterioplankton compositions of lakes and oceans: a first comparison based on fluorescence in situ hybridization. Appl Environ Microbiol 65: 3721–3726. PubMed PMC
Lindström ES, Kamst-Van Agterveld MP, Zwart G (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
Newton RJ, Jones SE, Eiler A, McMahon KD, Bertilsson S (2011) A guide to the natural history of freshwater lake bacteria. Microbiol Mol Biol Rev 75: 14–49. PubMed PMC
Hahn MW, Kasalický V, Jezbera J, Brandt U, Jezberová J, et al. (2010a) Limnohabitans curvus gen. nov, sp. nov, planktonic bacterium isolated from a freshwater lake. Int J Syst Evol Microbiol 60: 1358–1365. PubMed PMC
Glöckner FO, Zaichikov E, Belkova N, Denissova L, Pernthaler J, et al. (2000) Comparative 16S rRNA analysis of lake bacterioplankton reveals globally distributed phylogenetic clusters including an abundant group of Actinobacteria . Appl Environ Microb 66: 5053–5065. PubMed PMC
Hahn MW, Kasalický V, Jezbera J, Brandt U, Šimek K (2010) Limnohabitans australis sp. nov, isolated from a freshwater pond, and emended description of the genus Limnohabitans. . Int J Syst Evol Microbiol 60: 2946–2950. PubMed PMC
Kasalický V, Jezbera J, Šimek K, Hahn MW (2010) Limnohabitans planktonicus sp. nov. and Limnohabitans parvus sp. nov, planktonic betaproteobacteria isolated from a freshwater reservoir, and emended description of the genus Limnohabitans . Int J Syst Evol Microbiol 60: 2710–2714. PubMed PMC
Šimek K, Pernthaler J, Weinbauer MG, Horňák K, Dolan JR, et al. (2001) Changes in bacterial community composition, dynamics and viral mortality rates associated with enhanced flagellate grazing in a meso-eutrophic reservoir. Appl Environ Microbiol 67: 2723–2733. PubMed PMC
Zwart G, Crump BC, Kamst-van Agterveld MP, Hagen F, Han SK (2002) Typical freshwater bacteria: an analysis of available 16S rRNA gene sequences from plankton of lakes and rivers. Aquat Microb Ecol 28: 141–155.
Page KA, Connon SA, Giovannoni SJ (2004) Representative freshwater bacterioplankton isolated from Crater Lake, Oregon. Appl Environ Microbiol 70: 6542–6550. PubMed PMC
Šimek K, Kasalický V, Jezbera J, Jezberová J, Hejzlar J, et al. (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
Hörtnagl P, Pérez MT, Zeder M, Sommaruga R (2010) The bacterial community composition of the surface microlayer in a high mountain lake. FEMS Microbiol Ecol 73: 458–467. PubMed PMC
Buck U, Grossart HP, Amann R, Pernthaler J (2009) Substrate incorporation patterns of bacterioplankton populations in stratified and mixed waters of a humic lake. Environ Microbiol 11: 1854–1865. PubMed
Salcher MM, Pernthaler J, Posch T (2010) Spatiotemporal distribution and activity patterns of bacteria from three phylogenetic groups in an oligomesotrophic lake. Limnol Oceanogr 55: 846–856.
Šimek K, Horňák K, Jezbera J, Mašín M, Nedoma J, et al. (2005) Influence of top-down and bottom-up manipulations on the R-BT065 subcluster of b-proteobacteria, an abundant group in bacterioplankton of a freshwater reservoir. Appl Environ Microbiol 71: 2381–2390. PubMed PMC
Salcher MM, Hofer J, Horňák K, Jezbera J, Sonntag B, et al. (2007) Modulation of microbial predator-prey dynamics by phosphorus availability: growth patterns and survival strategies of bacterial phylogenetic clades. FEMS Microbiol Ecol 60: 40–50. PubMed
Horňák K, Jezbera J, Nedoma J, Gasol JM, Šimek K (2006) Effects of resource availability and bacterivory on leucine incorporation in different groups of freshwater bacterioplankton, assessed using microautoradiography. Aquat Microb Ecol 45: 277–289.
Salcher MM, Pernthaler J, Zeder M, Psenner R, Posch T (2008) Spatio-temporal niche separation of planktonic Betaproteobacteria in an oligo-mesotrophic lake. Environ Microbiol 10: 2074–2086. PubMed
Pérez MT, Hörtnagl P, Sommaruga R (2010) Contrasting ability to take up leucine and thymidine among freshwater bacterial groups: implications for bacterial production measurements. Environ Microbiol 12: 74–82. PubMed PMC
Šimek K, Horňák K, Jezbera J, Nedoma J, Vrba J, et al. (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, Weinbauer MG, Horňák K, Jezbera J, Nedoma J, et al. (2007) Grazer and virus-induced mortality of bacterioplankton accelerates development of Flectobacillus populations in a freshwater community. Environ Microbiol 9: 789–800. PubMed
Jezbera J, Horňák K, Šimek K (2006) Prey selectivity of bacterivorous protists in different size fractions of reservoir water amended with nutrients. Environ Microbiol 8: 1330–1339. PubMed
Šimek K, Kasalický V, Horňák K, Hahn MW, Weinbauer MG (2010) Assessing niche separation in coexisting Limnohabitans strains through interactions with a competitor, viruses, and a bacterivore. Appl Environ Microbiol 76: 1406–1416. PubMed PMC
Pérez MT, Sommaruga R (2006) Differential effect of algal- and soil-derived dissolved organic matter on alpine lake bacterial community composition and activity. Limnol Oceanogr 51: 2527–2537.
Šimek K, Horňák K, Jezbera J, Nedoma J, Znachor P, et al. (2008) Spatio-temporal patterns of bacterioplankton production and community composition related to phytoplankton composition and protistan bacterivory in a dam reservoir. Aquat Microb Ecol 51: 249–262.
Šimek K, Kasalický V, Zapomělová E, Horňák K (2011) Algal-derived substrates select for distinct betaproteobacterial lineages and contribute to niche separation in Limnohabitans strains. Appl Environ Microbiol 77: 7307–7315. PubMed PMC
Glaeser SP, Grossart H-P, Glaeser J (2010) Singlet oxygen, a neglected but important environmental factor: Short-term and long-term effects on bacterioplankton composition in a humic lake. Environ Microbiol 12: 3124–3136. PubMed
Zeng Y, Kasalický V, Šimek K, Koblížek M (2012) Genome sequences of two freshwater betaproteobacterial isolates, Limnohabitans species strains Rim28 and Rim47, indicate their capabilities as both photoautotrophs and ammonia oxidizers. J Bacteriol 194 (22): 6302 doi: 10.1128/JB.01481–12 PubMed DOI PMC
Eiler A, Heinrich F, Bertilsson S (2012) Coherent dynamics and association networks among lake bacterioplankton taxa. ISME J 6: 330–342. PubMed PMC
Mueller-Spitz SR, Goetz GW, McLellan SL (2009) Temporal and spatial variability in nearshore bacterioplankton communities of Lake Michigan. FEMS Microbiol Ecol 67: 511–522. PubMed
Fraune S, Bosch T (2007) Long-term maintenance of species-specific bacterial microbiota in the basal metazoan Hydra. Proc Natl Acad Sci U S A, 104, 13146–13151. PubMed PMC
Freese HM, Schink B (2011) Composition and stability of the microbial community inside the digestive tract of the aquatic crustacean Daphnia magna. Microb Ecol DOI 10.1007/s00248–011–9886–8. PubMed
Katoh K, Toh H (2008) Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9: 286–298. PubMed
Crump B, Kling G, Bahr M, Hobbie J (2003) Bacterioplankton community shifts in an Arctic lake correlate with seasonal changes in organic matter source. Appl Environ Microbiol 69: 2253–2268. PubMed PMC
Percent SF, Frischer ME, Vescio PA, Duffy EB, Milano V, et al. (2008) Bacterial community structure of acid-impacted lakes: what controls diversity? Appl Environ Microbiol 74: 1856–1868. PubMed PMC
Shaw AK, Halpern AL, Beeson K, Tran B, Venter JC, et al. (2008) It’s all relative: ranking the diversity of aquatic bacterial communities. Environ Microbiol 10: 2200–2210. PubMed
Hahn MW, Stadler P, Wu QL, Pöckl M (2004) The filtration-acclimatization-method for isolation of an important fraction of the not readily cultivable bacteria. J Microb Meth 57: 379–390. PubMed
Hahn MW, Pöckl M, Wu QL (2005) Low intraspecific diversity in a Polynucleobacter subcluster population numerically dominating bacterioplankton of a freshwater pond. Appl Environ Microbiol 71: 4539–4547. PubMed PMC
Hahn MW, Lang E, Brandt U, Wu QL, Scheuerl T (2009) Emended description of the genus Polynucleobacter and the species P. necessarius and proposal of two subspecies P necessarius subspecies necessarius subsp. nov. and P. necessarius subsp. asymbioticus subsp. nov. Int J Syst Evol Microbiol 59: 2002–2009. PubMed PMC
Wu QL, Hahn MW (2006) High predictability of the seasonal dynamics of a species-like Polynucleobacter population in a freshwater lake. Environ Microbiol 8: 1660–1666. PubMed
Hahn MW, Scheuerl T, Jezberová J, Koll U, Jezbera J, et al.. (2012) The passive yet successful way of planktonic life: genomic and experimental analysis of the ecology of a free-living Polynucleobacter population. PLoS One 7(3), e32772. PubMed PMC
Boyer SL, Flechtner VR, Johansen JR (2001) Is the 16S–23S rRNA internal transcribed spacer region a good tool for use in molecular systematics and population genetics? A case study in cyanobacteria. Mol Biol Evol 18: 1057–1069. PubMed
Risso C, Sun J, Zhuang K, Mahadevan R, DeBoy R, et al. (2009) Genome-scale comparison and constraint-based metabolic reconstruction of the facultative anaerobic Fe(III)-reducer Rhodoferax ferrireducens . BMC Genomics 10: 447. PubMed PMC
Stewart FJ, Cavanaugh CM (2007) Intragenomic variation and evolution of the internal transcribed spacer of the rRNA operon in bacteria. J Mol Evol 65: 44–67. PubMed
Wu QL, Peng X, Wen-Tso L (2010) East Tibetan Lakes Harbour Novel Clusters of Picocyanobacteria as Inferred from the 16S–23S rRNA Internal Transcribed Spacer Sequences. Microb Ecol 59: 614–622. PubMed
Hoffmann M, Brown EW, Feng PC, Keys CE, Fischer M, et al. (2010) PCR-based method for targeting 16S–23S rRNA intergenic spacer regions among Vibrio species. BMC Microbiol 10: 90 doi:10.1186/1471-2180-10-90 PubMed DOI PMC
Jezbera J, Jezberová J, Brandt U, Hahn MW (2011) Ubiquity of Polynucleobacter necessarius subspecies asymbioticus results from ecological diversification. Environ Microbiol 13: 922–931 doi:10.1111/j.1462-2920.2010.02396.x PubMed DOI PMC
Stackebrandt E, Ebers J (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiology Today, 152–155.
Galperin MY (2005) A census of membrane-bound and intracellular signal transduction proteins in bacteria: Bacterial IQ, extroverts and introverts. BMC Microbiol 5: 35. PubMed PMC
Yooseph S, Nealson KH, Rusch DB, McCrow JP, Dupont CL, et al. (2010) Genomic and functional adaptation in surface ocean planktonic prokaryotes. Nature 468: 60–66. PubMed
Giroldo D, Vieira AAH (2002) An extracellular sulphated fucose-rich polysaccharides produced by a tropical strain of C. obovata (Cryptophyceae). J Appl Phycol 14: 185–191.
Giroldo D, Vieira AAH (2005) Polymeric and free sugars released by three phytoplanktonic species from a freshwater tropical eutrophic reservoir. Journal of Plankton Research 27: 695–705.
Grossart HP, Levold F, Allgaier M, Simon M, Brinkhoff T (2005) Marine diatom species harbour distinct bacterial communities. Environ Microbiol 7: 860–873. PubMed
Horňák K, Jezbera J, Šimek K (2008) Effects of a Microcystis aeruginosa bloom and bacterivory on bacterial abundance and activity in a eutrophic reservoir. Aquat Microb Ecol 52: 107–117.
Alonso C, Zeder M, Piccini C, Conde D, Pernthaler J (2009) Ecophysiological differences of betaproteobacterial populations in two hydrochemically distinct compartments of a subtropical lagoon. Environ Microbiol 11: 867–876. PubMed
Boenigk J, Stadler P, Wiedlroither A, Hahn MW (2004) Strain-specific differences in the grazing sensitivities of closely related ultramicrobacteria affiliated with the Polynucleobacter cluster. Appl Environ Microbiol 70: 5787–5793. PubMed PMC
Vannini C, Pöckl M, Petroni G, Wu QL, Lang E, et al. (2007) Endosymbiosis in statu nascendi: Close phylogenetic relationship between obligately endosymbiotic and obligately free-living Polynucleobacter strains (Betaproteobacteria). Environ Microbiol 9: 347–359. PubMed
Urbanczyk H, Ast JC, Higgins MJ, Carson J, Dunlap PV (2007) Reclassification of Vibrio fischeri, Vibrio logei, Vibrio salmonicida and Vibrio wodanis as Aliivibrio fischeri gen. nov, comb. nov, Aliivibrio logei comb. nov, Aliivibrio salmonicida comb. nov. and Aliivibrio wodanis comb. nov. Int J Syst Evol Microbiol 57: 2823–2829. PubMed
Manz W, Amann R, Ludwig W, Wagner M, Schleifer K-H (1992) Phylogenetic oligodeoxynucleotide probes for the major subclasses of Proteobacteria: problems and solutions. Syst Appl Microbiol 15: 593–600.
Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173: 697–703. PubMed PMC
Lane DJ, Pace B, Olsen GJ (1985) Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc Natl Acad Sci USA 82: 6955–6959. PubMed PMC
Fisher MM, Triplett EW (1999) Automated approach for ribosomal intergenic spacer analysis of microbial diversity and its application to freshwater bacterial communities. Appl Environ Microbiol 65: 4630–4636. PubMed PMC
Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30: 3059–3066. PubMed PMC
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41: 95–98.
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol Biol Evol 28: 2731–2739. PubMed PMC
Posada D (2008) jModelTest: Phylogenetic Model Averaging. Mol Biol Evol 25: 1253–1256. PubMed
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696–704. PubMed
Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17: 754–755. PubMed
Ludwig W, Strunk O, Westram R, Richter L, Meier H, et al. (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32(4): 1363–1371. PubMed PMC
Posch T, Pernthaler J, Alfreider A, Psenner A (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
Posch T, Franzoi J, Prader M, Salcher MM (2009) New image analysis tool to study biomass and morphotypes of three major bacterioplankton groups in an alpine lake. Aquat Microb Ecol 54: 113–126.
Loferer-Krössbacher M, Klima J, Psenner R (1998) Determination of bacterial cell dry mass by transmission electron microscopy and densitometric image analysis. Appl Environ Microbiol 64: 688–694. PubMed PMC
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