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Temporal Patterns in Glycolate-Utilizing Bacterial Community Composition Correlate with Phytoplankton Population Dynamics in Humic Lakes

  • Microbiology of Aquatic Systems
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Abstract

Previous observations of correlated community dynamics between phytoplankton and bacteria in lakes indicate that phytoplankton populations may influence bacterial community structure. To investigate the possibility that bacterial use of phytoplankton exudates contributes to observed patterns of community change, we characterized the diversity and dynamics of heterotrophic bacterioplankton with genetic potential to use glycolate, a photorespiration-specific exudate, in five lakes over a 15-week period. Culture-independent approaches were used to track different bacterial phylotypes represented by DNA sequence variation in the functional gene glycolate oxidase subunit D (glcD). glcD gene sequences from freshwater bacteria exhibited broad phylogenetic diversity, including sequences representing the Alpha-, Beta-, and Gammaproteobacteria, Actinobacteria, Bacteroidetes, Firmicutes, and Verrucomicrobia. The majority of glcD gene sequences were betaproteobacterial, with 48% of the sequences clustering with the glcD gene from the cosmopolitan freshwater species Polynucleobacter necessarius. Terminal restriction fragment length polymorphism fingerprinting of the glcD gene revealed changes in glycolate-utilizing assemblages over time. An average of 39% of within-lake temporal variation in glycolate-utilizing assemblages across five lakes was explained by phytoplankton community composition and dynamics. The interaction between phytoplankton populations and the environment explained an additional 17% of variation on average. These observations offer new insight into the diversity and temporal dynamics of freshwater bacteria with genetic potential to use glycolate and support the hypothesis that algal exudates influence the structure of bacterial communities.

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References

  1. Cole JJ, Findlay S, Pace ML (1988) Bacterial production in fresh and saltwater ecosystems: a cross-system overview. Mar Ecol Prog Ser 43:1–10

    Article  Google Scholar 

  2. Cotner JB, Biddanda BA (2002) Small players, large role: microbial influence on biogeochemical processes in pelagic aquatic ecosystems. Ecosystems 5:105–121

    Article  CAS  Google Scholar 

  3. Cole JJ (1982) Interactions between bacteria and algae in aquatic ecosystems. Ann Rev Ecolog Syst 13:291–314

    Article  Google Scholar 

  4. Azam F, Fenchel T, Field JG, Gray JS, Meyerreil LA, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263

    Article  Google Scholar 

  5. White PA, Kalff J, Rasmussen JB, Gasol JM (1991) The effect of temperature and algal biomass on bacterial production and specific growth-rate in fresh-water and marine habitats. Microb Ecol 21:99–118

    Article  Google Scholar 

  6. Kent AD, Jones SE, Lauster GH, Graham JM, Newton RJ, McMahon KD (2006) Experimental manipulations of microbial food web interactions in a humic lake: shifting biological drivers of bacterial community structure. Environ Microbiol 8:1448–1459

    Article  CAS  PubMed  Google Scholar 

  7. Pinhassi J, Sala MM, Havskum H, Peters F, Guadayol O, Malits A, Marrase CL (2004) Changes in bacterioplankton composition under different phytoplankton regimens. Appl Environ Microbiol 70:6753–6766

    Article  CAS  PubMed  Google Scholar 

  8. Kent AD, Jones SE, Yannarell AC, Graham JM, Lauster GH, Kratz TK, Triplett EW (2004) Annual patterns in bacterioplankton community variability in a humic lake. Microb Ecol 48:550–560

    Article  CAS  PubMed  Google Scholar 

  9. Kent AD, Yannarell AC, Rusak JA, Triplett EW, McMahon KD (2007) Synchrony in aquatic microbial community dynamics. ISME J 1:38–47

    Article  CAS  PubMed  Google Scholar 

  10. Rooney-Varga JN, Giewat MW, Savin MC, Sood S, LeGresley M, Martin JL (2005) Links between phytoplankton and bacterial community dynamics in a coastal marine environment. Microb Ecol 49:163–175

    Article  CAS  PubMed  Google Scholar 

  11. Bertilsson S, Eiler A, Nordqvist A, Jorgensen NOG (2007) Links between bacterial production, amino-acid utilization and community composition in productive lakes. ISME J 1:532–544

    Article  CAS  PubMed  Google Scholar 

  12. Ishida CK, Arnon S, Peterson CG, Kelly JJ, Gray KA (2008) Influence of algal community structure on denitrification rates in periphyton cultivated on artificial substrata. Microb Ecol 56:140–152

    Article  PubMed  Google Scholar 

  13. Strickland MS, Osburn E, Lauber C, Fierer N, Bradford MA (2009) Litter quality is in the eye of the beholder: initial decomposition rates as a function of inoculum characteristics. Funct Ecol 23:627–636

    Article  Google Scholar 

  14. Wu QLL, Hahn MW (2006) High predictability of the seasonal dynamics of a species-like Polynucleobacter population in a freshwater lake. Environ Microbiol 8:1660–1666

    Article  CAS  PubMed  Google Scholar 

  15. LaPara TM, Konopka A, Nakatsu CH, Alleman JE (2000) Effects of elevated temperature on bacterial community structure and function in bioreactors treating a synthetic wastewater. J Ind Microbiol Biotechnol 24:140–145

    Article  CAS  Google Scholar 

  16. Jardillier L, Boucher D, Personnic S, Jacquet S, Thenot A, Sargos D, Amblard C, Debroas D (2005) Relative importance of nutrients and mortality factors on prokaryotic community composition in two lakes of different trophic status: microcosm experiments. FEMS Microbiol Ecol 53:429–443

    Article  CAS  PubMed  Google Scholar 

  17. Strecker AL, Cobb TP, Vinebrooke RD (2004) Effects of experimental greenhouse warming on phytoplankton and zooplankton communities in fishless alpine ponds. Limnol Oceanogr 49:1182–1190

    Article  CAS  Google Scholar 

  18. Tilman D, Kilham SS, Kilham P (1982) Phytoplankton community ecology—the role of limiting nutrients. Ann Rev Ecolog Syst 13:349–372

    Article  Google Scholar 

  19. Larsson U, Hagstrom A (1979) Phytoplankton exudate release as an energy source for the growth of pelagic bacteria. Mar Biol 52:199–206

    Article  Google Scholar 

  20. Baines SB, Pace ML (1991) The production of dissolved organic matter by phytoplankton and its importance to bacterial patterns across marine and freshwater systems. Limnol Oceanogr 36:1078–1090

    Article  Google Scholar 

  21. Brock TD, Clyne J (1984) Significance of algal excretory products for growth of epilimnetic bacteria. Appl Environ Microbiol 47:731–734

    CAS  PubMed  Google Scholar 

  22. Hellebust JA (1965) Excretion of some organic compounds by marine phytoplankton. Limnol Oceanogr 10:192–206

    Article  Google Scholar 

  23. Fogg GE (1983) The ecological significance of extracellular products of phytoplankton photosynthesis. Bot Mar 26:3–14

    Article  CAS  Google Scholar 

  24. Myklestad SM (1995) Release of extracellular products of phytoplankton with special emphasis on polysaccharides. Sci Total Environ 165:155–164

    Article  CAS  Google Scholar 

  25. Parker MS, Armbrust EV (2005) Synergistic effects of light, temperature, and nitrogen source on transcription of genes for carbon and nitrogen metabolism in the centric diatom Thalassiosira pseudonana (Bacillariophyceae). J Phycol 41:1142–1153

    Article  CAS  Google Scholar 

  26. Hama T, Honjo T (1987) Photosynthetic products and nutrient availability in phytoplankton population from Gokasho Bay, Japan. J Exp Mar Biol Ecol 112:251–266

    Article  CAS  Google Scholar 

  27. Morris I, Skea W (1978) Products of photosynthesis in natural populations of marine phytoplankton for Gulf of Maine. Mar Biol 47:303–312

    Article  CAS  Google Scholar 

  28. Panzenbock M (2007) Effect of solar radiation on photosynthetic extracellular carbon release and its microbial utilization in alpine and Arctic lakes. Aquat Microb Ecol 48:155–168

    Article  Google Scholar 

  29. Anneville O, Souissi S, Ibanez F, Ginot V, Druart JC, Angeli N (2002) Temporal mapping of phytoplankton assemblages in Lake Geneva: annual and interannual changes in their patterns of succession. Limnol Oceanogr 47:1355–1366

    Article  Google Scholar 

  30. Graham JM, Kent AD, Lauster GH, Yannarell AC, Graham LE, Triplett EW (2004) Seasonal dynamics of phytoplankton and planktonic protozoan communities in a northern temperate humic lake: diversity in a dinoflagellate dominated system. Microb Ecol 48:528–540

    Article  CAS  PubMed  Google Scholar 

  31. Zhang X, Xie P, Chen FZ, Li SX, Qin JH (2007) Driving forces shaping phytoplankton assemblages in two subtropical plateau lakes with contrasting trophic status. Freshw Biol 52:1463–1475

    Article  CAS  Google Scholar 

  32. Charpin MF, Maurin N, Amblard C, Devaux J (1998) Seasonal variations of phytoplankton photosynthate partitioning in two lakes of different trophic level. J Plankton Res 20:901–921

    Article  Google Scholar 

  33. Judd KE, Crump BC, Kling GW (2006) Variation in dissolved organic matter controls bacterial production and community composition. Ecology 87:2068–2079

    Article  PubMed  Google Scholar 

  34. Nelson CE (2009) Phenology of high-elevation pelagic bacteria: the roles of meteorologic variability, catchment inputs and thermal stratification in structuring communities. ISME J 3:13–30

    Article  CAS  PubMed  Google Scholar 

  35. Crump BC, Kling GW, Bahr M, Hobbie JE (2003) Bacterioplankton community shifts in an arctic lake correlate with seasonal changes in organic matter source. Appl Environ Microbiol 69:2253–2268

    Article  PubMed  Google Scholar 

  36. Jones SE, Newton RJ, McMahon KD (2009) Evidence for structuring of bacterial community composition by organic carbon source in temperate lakes. Environ Microbiol 11:2463–2472

    Article  CAS  PubMed  Google Scholar 

  37. Puddu A, Zoppini A, Fazi S, Rosati M, Amalfitano S, Magaletti E (2003) Bacterial uptake of DOM released from P-limited phytoplankton. FEMS Microbiol Ecol 46:257–268

    Article  CAS  PubMed  Google Scholar 

  38. Grossart HP, Levold F, Allgaier M, Simon M, Brinkhoff T (2005) Marine diatom species harbour distinct bacterial communities. Environ Microbiol 7:860–873

    Article  CAS  PubMed  Google Scholar 

  39. Oliver DJ (1998) Photorespiration and the C2 cycle. In: Raghavendra AS (ed) Photosynthesis: a comprehensive treatise. Cambridge University Press, New York, pp 173–182

    Google Scholar 

  40. Ornston LN, Ornston MK (1969) Regulation of glycolate metabolism in Escherichia coli K-12. J Bacteriol 98:1098–1108

    CAS  PubMed  Google Scholar 

  41. Lord JM (1972) Glycolate oxidoreductase in Escherichia coli. Biochim Biophys Acta 267:227–237

    Article  CAS  PubMed  Google Scholar 

  42. Wright RT, Shah NM (1975) Trophic role of glycolic acid in coastal seawater 1: heterotrophic metabolism in seawater and bacterial cultures. Mar Biol 33:175–183

    Article  CAS  Google Scholar 

  43. Lau WWY, Armbrust EV (2006) Detection of glycolate oxidase gene glcD diversity among cultured and environmental marine bacteria. Environ Microbiol 8:1688–1702

    Article  CAS  PubMed  Google Scholar 

  44. Lau WWY, Keil RG, Armbrust EV (2007) Succession and diel transcriptional response of the glycolate-utilizing component of the bacterial community during a spring phytoplankton bloom. Appl Environ Microbiol 73:2440–2450

    Article  CAS  PubMed  Google Scholar 

  45. Drummond AJ, Ashton B, Cheung M, Heled J, Kearse M, Stones-Havas S, Thierer T, Wilson A (2009) Geneious v4.7. Available from http://www.geneious.com

  46. Marchler-Bauer A, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, Gwadz M, He S, Hurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Liebert CA, Liu C, Lu F, Lu S, Marchler GH, Mullokandov M, Song JS, Tasneem A, Thanki N, Yamashita RA, Zhang D, Zhang N, Bryant SH (2009) CDD: specific functional annotation with the Conserved Domain Database. Nucleic Acids Res 37:D205–D210

    Article  CAS  PubMed  Google Scholar 

  47. Hudson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267

    Article  Google Scholar 

  48. Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71:1501–1506

    Article  CAS  PubMed  Google Scholar 

  49. Felsenstein J (2005) PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle

  50. Kalendar R, Lee D, Schulman A (2009) FastPCR software for PCR primer and probe design in complete search. Genes, Genomes, and Genomics 3:1–14

    Google Scholar 

  51. Fierer N, Schimel JP, Holden PA (2003) Influence of drying-rewetting frequency on soil bacterial community structure. Microb Ecol 45:63–71

    Article  CAS  PubMed  Google Scholar 

  52. Peralta AL, Matthews JW, Kent AD (2010) Microbial community structure and denitrification in a wetland mitigation bank. Appl Environ Microbiol 76:4207–4215

    Article  CAS  PubMed  Google Scholar 

  53. Legandre P, Legandre L (1998) Numerical ecology. Elsevier, New York

    Google Scholar 

  54. Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation. PRIMER-E Ltd, Plymouth

    Google Scholar 

  55. ter Braak CJF, Smilauer P (2002) CANOCO reference manual and CanoDraw for Windows user's guide: software for canonical community ordination (version 4.5). Microcomputer Power, Ithaca

    Google Scholar 

  56. Ruan QS, Dutta D, Schwalbach MS, Steele JA, Fuhrman JA, Sun FZ (2006) Local similarity analysis reveals unique associations among marine bacterioplankton species and environmental factors. Bioinformatics 22:2532–2538

    Article  CAS  PubMed  Google Scholar 

  57. Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci USA 100:9440–9445

    Article  CAS  PubMed  Google Scholar 

  58. Shade A, Chiu CY, McMahon KD (2010) Differential bacterial dynamics promote emergent community robustness to lake mixing: an epilimnion to hypolimnion transplant experiment. Environ Microbiol 12:455–466

    Article  CAS  PubMed  Google Scholar 

  59. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504

    Article  CAS  PubMed  Google Scholar 

  60. Burkert U, Warnecke F, Babenzien D, Zwirnmann E, Pernthaler J (2003) Members of a readily enriched beta-proteobacterial clade are common in surface waters of a humic lake. Appl Environ Microbiol 69:6550–6559

    Article  CAS  PubMed  Google Scholar 

  61. Newton RJ, Kent AD, Triplett EW, McMahon KD (2006) Microbial community dynamics in a humic lake: differential persistence of common freshwater phylotypes. Environ Microbiol 8:956–970

    Article  PubMed  Google Scholar 

  62. Forney LJ, Zhou X, Brown CJ (2004) Molecular microbial ecology: land of the one-eyed king. Curr Opin Microbiol 7:210–220

    Article  CAS  PubMed  Google Scholar 

  63. Zwart G, Crump BC, Agterveld M, 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

    Article  Google Scholar 

  64. Vannini C, Pockl M, Petroni G, Wu QLL, Lang E, Stackebrandt E, Schrallhammer M, Richardson PM, Hahn MW (2007) Endosymbiosis in statu nascendi: close phylogenetic relationship between obligately endosymbiotic and obligately free-living Polynucleobacter strains (Betaproteobacteria). Environ Microbiol 9:347–359

    Article  CAS  PubMed  Google Scholar 

  65. Hahn MW, Pockl M, Wu QLL (2005) Low intraspecific diversity in a Polynucleobacter subcluster population numerically dominating bacterioplankton of a freshwater pond. Appl Environ Microbiol 71:4539–4547

    Article  CAS  PubMed  Google Scholar 

  66. 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

    Article  PubMed  Google Scholar 

  67. Newton RJ, Jones SE, Helmus MR, McMahon KD (2007) Phylogenetic ecology of the freshwater Actinobacteria acI lineage. Appl Environ Microbiol 73:7169–7176

    Article  CAS  PubMed  Google Scholar 

  68. Warnecke F, Sommaruga R, Sekar R, Hofer JS, Pernthaler J (2005) Abundances, identity, and growth state of actinobacteria in mountain lakes of different UV transparency. Appl Environ Microbiol 71:5551–5559

    Article  CAS  PubMed  Google Scholar 

  69. Allgaier M, Grossart HP (2006) Diversity and seasonal dynamics of Actinobacteria populations in four lakes in northeastern Germany. Appl Environ Microbiol 72:3489–3497

    Article  CAS  PubMed  Google Scholar 

  70. Sachse A, Babenzien D, Ginzel G, Gelbrecht J, Steinberg CEW (2001) Characterization of dissolved organic carbon (DOC) in a dystrophic lake and an adjacent fen. Biogeochemistry 54:279–296

    Article  CAS  Google Scholar 

  71. R Development Core Team (2007). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org

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Acknowledgments

We thank Y. Chang for assistance with molecular analyses; A. Yannarell, S. Jones, and A. Shade for assistance with sequence and statistical analysis programs; and C. Cáceres, D. Keymer, M. Lemke, K. McMahon, A. Peralta, A. Shade, R. Whitaker, A. Yannarell, and anonymous reviewers for thoughtful comments on this manuscript. Funding for this work was provided by NSF grant MCB 0702653 and an O’Dell Fellowship from the University of Illinois to S.F.P.

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Correspondence to Angela D. Kent.

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Paver, S.F., Kent, A.D. Temporal Patterns in Glycolate-Utilizing Bacterial Community Composition Correlate with Phytoplankton Population Dynamics in Humic Lakes. Microb Ecol 60, 406–418 (2010). https://doi.org/10.1007/s00248-010-9722-6

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