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Changes in Pelagic Bacteria Communities Due to Leaf Litter Addition

  • Environmental Microbiology
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Abstract

In many limnetic systems, the input of allochthonous organic matter, e.g., leaf litter, is a substantial source of dissolved organic carbon (DOC) for pelagic bacteria, especially in fall and winter when autochthonous DOC production is low. However, relatively little is known about community changes of pelagic lake bacteria due to leaf litter input which includes both the release of leaf leachates and microorganisms from the leaf litter into the surrounding water. Therefore, we have experimentally studied the effects of different types of leaf litter (Betula pendula, Fagus silvatica, and Pinus silvestris) on the pelagic bacterial community composition by adding leaves to different treatments of epilimnic water samples (unfiltered, 0.2 µm and 5.0 µm-pre-filtered) from humic Lake Grosse Fuchskuhle (Northeastern Germany). The addition of leaf litter led to a significant increase in DOC concentration in lake water, and each leaf litter type produced significantly different amounts of DOC (p = <0.001) as well as of specific DOC fractions (p = <0.001), except of polysaccharides. DGGE banding patterns varied over time, between types of leaf litter, and among treatments. Bacteria belonging to known bacterial phylotypes in the southwest basin of Lake Grosse Fuchskuhle were frequently found and even persisted after leaf litter additions. Upon leaf litter addition, α-proteobacteria (Azospirillum, Novosphingobium, and Sphingopyxis) as well as β-proteobacteria (Curvibacter and Polynucleobacter) were enriched. Our results indicate that supply of leaf litter DOM shifted the bacterial community in the surrounding water towards specific phylotypes including species capable of assimilating the more recalcitrant DOC pools. Statistical analyses, however, show that DGGE banding patterns are not only affected by DOC pools but also by treatment. This indicates that biological factors such as source community and grazing may be also important for shifts in bacterial community structure following leaf litter input into different lakes.

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References

  1. Hieber M, Gessner MO (2002) Contribution of stream detritivores, fungi, and bacteria to leaf breakdown based on biomass estimates. Ecol 83:1026–1038

    Article  Google Scholar 

  2. Gessner MO (1999) Aquatische Hyphomyceten. In: Tümpling Wv, Friedrich G (eds) Biologische Gewässeruntersuchung. G. Fischer, Jena, pp 185–198

    Google Scholar 

  3. Gessner MO, Chauvet E, Dobson M (1999) A perspective on leaf litter breakdown in streams. Oikos 85:377–384

    Article  Google Scholar 

  4. Suberkropp K, Arsuffi TL, Anderson JP (1983) Comparison of degradative availability enzymatic activity, and palatability of aquatic hyphomycetes grown on leaf litter. Appl Environ Microbiol 46:237–244

    CAS  PubMed  Google Scholar 

  5. Baldy V, Gessner MO (1997) Towards a budget of leaf litter decomposition in a first-order woodland stream. C R’Acad Sci Sér III 320:747–758

    Google Scholar 

  6. Findlay SEG, Arsuffi TL (1989) Microbial growth and detritus transformations during decomposition of leaf litter in a stream. Freshw Biol 21:261–270

    Article  Google Scholar 

  7. Baldy V, Chauvet E, Charcosset J-Y, Gessner MO (2002) Microbial dynamics associated with leaves decomposing in the mainstem and floodplain pond of a large river. Aquat Microb Ecol 28:25–36

    Article  Google Scholar 

  8. Meyer JL, Wallace JB, Eggert SL (1998) Leaf litter as a source of dissolved organic carbon in streams. Ecosystems 1:240–249

    Article  CAS  Google Scholar 

  9. Wiegner TN, Kaplan LA, Newbold JD (2005) Contribution of dissolved organic C to stream metabolism: a mesocosm study using 13C-enriched tree-tissue leachate. J N Am Benthol Soc 24:48–67

    Article  Google Scholar 

  10. Tranvik L (1998) Degradation of dissolved organic matter in humic waters by bacteria. Aquatic Humic Substances: Ecology and Biogeochemistry. Ecological Studies, Vol 133 (Hessen DO & Tranvik LJ, eds), pp 9–39. Springer, Berlin

  11. Søndergaard M, Middelboe M (1995) A cross-system analysis of labile dissolved organic carbon. Mar Ecol Prog Ser 118:283–294

    Article  Google Scholar 

  12. Bohman IM, Tranvik LJ (2001) The effects of shredding invertebrates on the transfer of organic carbon from littoral leaf litter to water-column bacteria. Aquat Ecol 35:43–50

    Article  Google Scholar 

  13. Pope RJ, Gordon AM, Kaushik NK (1999) Leaf litter colonization by invertebrates in the littoral zone of a small oligotrophic lake. Hydrobiologia 392:99–112

    Article  Google Scholar 

  14. Leff LG, Meyer JL (1991) Biological availability of dissolved organic carbon along the Ogeechee river. Limnol Oceanogr 36:315–323

    Article  CAS  Google Scholar 

  15. McDowell WH, Fisher SG (1976) Autumnal processing of dissolved organic matter in a small woodland stream. Ecol 57:561–569

    Article  Google Scholar 

  16. Loisel P, Harmand J, Zemb O, Latrille E, Lobry C, Delgenes JP, Godon JJ (2006) Denaturing gradient electrophoresis (DGE) and single-strand conformation polymorphism (SSCP) molecular fingerprintings revisited by simulation and used as a tool to measure microbial diversity. Environ Microbiol 8:720–731

    Article  CAS  PubMed  Google Scholar 

  17. Sachse A, Babenzien D, Ginzel G, Albrecht 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 

  18. Kasprzak P (1993) The use of an artificial divided bog lake in food-web studies. Verh Int Ver Limnol 25:652–656

    Google Scholar 

  19. Koschel R (1995) Manipulation of whole lake ecosystems and long term limnological observations of the Brandenburg-Mecklenburg lake district. Int Rev Gesamten Hydrobiol 80:1–12

    Article  Google Scholar 

  20. Allgaier M, Grossart H-P (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 

  21. Babenzien D, Babenzien C (1990) Microbial activities in a naturally acidotrophic lake. Arch Hydrobiol Suppl 34:175–181

    CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  23. Grossart H-P, Jezbera J, Hornak K, Hutalle KML, Buck U, Simek K (2008) Abundance and in situ activities of major bacterial groups in Lake Grosse Fuchskuhle (Northeastern Germany). Environ Microbiol 10:635–652

    Article  CAS  PubMed  Google Scholar 

  24. Huber SA, Frimmel FH (1996) Size-exclusion-chromatography with organic carbon detection (LC-OCD): A fast and reliable method for the characterization of hydrophilic organic matter in natural waters. Vom Wasser 86:277–290

    CAS  Google Scholar 

  25. Sekar R, Pernthaler A, Pernthaler J, Warnecke F, Posch T, Amann R (2003) An improved protocol for quantification of freshwater Actinobacteria by flourescence in situ hybridization. Appl Environ Microbiol 69:2928–2935

    Article  CAS  PubMed  Google Scholar 

  26. Daims H, Bruhl A, Amann R, Schleifer KH, Wagner M (1999) The domain-specific probe EUB338 is insufficient for the detection of all bacteria: development and evaluation of a more comprehensive probe set. Syst Appl Microbiol 22:434–444

    CAS  PubMed  Google Scholar 

  27. 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  Google Scholar 

  28. 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

    Google Scholar 

  29. Hutalle-Schmelzer KML, Grossart H-P (2009) Changes in bacterioplankton community of oligotrophic Lake Stechlin (northeastern Germany) after humic matter addition. Aquat Microb Ecol 55:155–168

    Article  Google Scholar 

  30. Zwart G, Crump B, MPKv A, Hagen F, Han S-K (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 

  31. Hahn MW (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

    Article  CAS  PubMed  Google Scholar 

  32. Bano N, Moran MA, Hodson RE (1998) Photochemical formation of labile organic matter from two components of dissolved organic carbon in a freshwater wetland. Aquat Microb Ecol 16:95–102

    Article  Google Scholar 

  33. Bertilsson S, Allard B (1996) Sequential photochemical and microbial degradation of refractory dissolved organic matter in a humic freshwater system. Arch Hydrobiol Spec Issues Advanc Limnol 48:133–141

    CAS  Google Scholar 

  34. Gessner MO, Chauvet E (1994) Importance of stream microfungi in controlling breakdown rates of leaf litter. Ecology 75:1807–1817

    Article  Google Scholar 

  35. Wehr JD, Petersen J, Findlay S (1998) Influence of three contrasting detrital carbon sources on planktonic bacterial metabolism in a mesotrophic lake. Microb Ecol 37:23–35

    Article  Google Scholar 

  36. 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 

  37. Glöckner F, Zaichikov E, Belkova N, Denissova L, Pernthaler J, Pernthaler A, Amann R (2000) Comparative 16 S rRNA analysis of lake bacterioplankton reveals globally distributed phylogenetic clusters including an abundant group of Actinobacteria. Appl Environ Microbiol 66:5053–5065

    Article  PubMed  Google Scholar 

  38. 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 

  39. Basta T, Buerger S, Stolz A (2005) Structural and replicative diversity of large plasmids from sphingomonads that degrade polycyclic aromatic compounds and xenobiotics. Microbiol 151:2025–2037

    Article  CAS  Google Scholar 

  40. Crump BC, Armbrust EV, Baross JA (1999) Phylogenetic analysis of particle-attached and free-living bacterial communities in the Columbia River, its estuary, and the adjacent coastal Ocean. Appl Environ Microbiol 65:3192–3204

    CAS  PubMed  Google Scholar 

  41. Méthe BA, Hiorns WD, Zehr JP (1998) Contrasts between marine and freshwater bacterial community composition: analysis of communities in Lake George and six other Adirondack lakes. Limnol Oceanogr 43:368–374

    Article  Google Scholar 

  42. Ding L, Yakota A (2004) Proposals of Curvibacter gracilis gen. nov., sp. nov. and Herbaspirillum putei sp. nov. for bacterial strains isolated from well water and reclassification of (Pseudomonas) huttiensis, (Pseudomonas) lanceolata, (Aquaspirillum) delicatum and (Aquaspirillum) autotrophicum as Herbaspirillum huttiense comb. nov., Curvibacter lanceolatus comb. nov., Curvibacter delicates comb. nov. and Herbaspirillum autotrophicum comb. nov. Int J Syst Evol Microbiol 54:2223–2230

    Article  CAS  PubMed  Google Scholar 

  43. Nold S, Zwart G (1998) Patterns and groverning forces in aquatic microbial communities. Aquat Ecol 32:17–35

    Article  CAS  Google Scholar 

  44. Lydell C, Dowell L, Sikaroodi M, Gillevet P, Emerson D (2004) A population survey of the members of the phylum Bacteroidetes isolated from salt marsh sediments along the east coast of the United States. Microb Ecol 48:263–273

    Article  CAS  PubMed  Google Scholar 

  45. He J, Zu Z, Hughes J (2006) Molecular bacterial diversity of a forest soil under residue management regimes in subtropical Australia. FEMS Microbiol Ecol 55:38–47

    Article  CAS  PubMed  Google Scholar 

  46. Beier S, Witzel KP, Marxsen J (2008) Bacterial community composition in central Europe running waters examined by temperature gradient gel electrophoresis and sequence analysis of 16S rRNA genes. Appl Environ Microbiol 74:188–199

    Article  CAS  PubMed  Google Scholar 

  47. Quaiser A, Ochsenreiter T, Lanz C, Schuster SC, Treusch AH, Eck J, Schleper C (2003) Acidobacteria form a coherent but highly diverse group within the bacterial domain: evidence from environmental genomics. Mol Microbiol 50:563–575

    Article  CAS  PubMed  Google Scholar 

  48. Kleinstueber S, Müller FD, Chatzinotas A, Wendt-Potthoff K, Harms H (2008) Diversity and in situ quantification of Actinobacteria subdivision 1 in an acidic mining lake. FEMS Microbiol Ecol 63:107–117

    Article  Google Scholar 

  49. Chen TY, Paulitsch M (1974) Inhaltstoffe von Nadeln, Rinde und Holz der Fichte und Kiefer und ihr Einfluss auf die Eigenschaften daraus hergestellter Spanplatten. Holz als Roh und Werkstoff. Springer-Verlag, Berlin, pp 397–401

    Google Scholar 

  50. Newton R, Kent A, Triplett E, McMahon K (2006) Microbial community dynamics in a humic lake: Differential persistence of a common freshwater phylotypes. Environ Microbiol 8:956–970

    Article  PubMed  Google Scholar 

  51. Moran MA, Hodson RE (1990) Bacterial production on humic and nonhumic components of dissolved organic carbon. Limnol Oceangr 35:1744–1756

    Article  CAS  Google Scholar 

  52. Suberkropp K, Klug MJ (1976) Fungi and bacteria associated with leaves during processing in a woodland stream. Ecol 57:707–719

    Article  Google Scholar 

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Acknowledgments

We thank E. Mach for the technical assistance during sampling and for the measurement of dissolved organic carbon, Sonja Raub for many useful comments in writing the first version of this manuscript, and Sarah Poynton for the language and manuscript revisions. This work was supported by a PhD scholarship to KMLHS from the Deutscher Akademischer Austauschdienst (DAAD), a course travel grant from Boehringer Ingelheim Fonds given to KMLHS, and by the Leibniz Foundation.

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Authors and Affiliations

  1. Department of Stratified Lakes, Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Alte Fischerhuette 2, 16775, Stechlin, Germany

    Kristine Michelle L. Hutalle-Schmelzer & Hans-Peter Grossart

  2. Department of Biological Sciences, College of Science, University of Santo Tomas, España St., Manila, 1008, Philippines

    Kristine Michelle L. Hutalle-Schmelzer

  3. Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Müggelseedamm 310, 12587, Berlin, Germany

    Elke Zwirnmann & Angela Krüger

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  1. Kristine Michelle L. Hutalle-Schmelzer
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  3. Angela Krüger
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  4. Hans-Peter Grossart
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Correspondence to Hans-Peter Grossart.

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ESM Table 1

Phylogenetic affiliation of sequenced DGGE bands in a) Betula—Betula pendula, b) Fagus—Fagus silvatica, c) Pinus—Pinus silvestris additions over a 28-day period, and d comparison of the BCC in Betula, Fagus, and Pinus additions at the end of the incubation. α (Alphaproteobacteria), β (Betaproteobacteria), γ (Gammaproteobacteria), B (Bacteroidetes), Ad (Acidobacteria), and C (Cyanobacteria). Accession numbers of the sequenced DGGE bands as well as a brief description,% similarity, and accession numbers of the nearest published relative and the nearest isolate relative (based on NCBI results) are given (DOC 194 kb)

ESM Fig. 1

DGGE gels of temporal changes in BCC after addition of a) Betula—Betula pendula, b) Fagus—Fagus silvatica, c) Pinus—Pinus silvestris additions at the end of the incubation. T 0 = time zero, FL = free-living bacteria, PA = particle-associated bacteria. α (Alphaproteobacteria), β (Betaproteobacteria), γ (Gammaproteobacteria), B (Bacteroidetes), Ad (Acidobacteria), and C (Cyanobacteria). Sequenced bands are marked by arrows and their respective band numbers. Detailed phylogenetic characterizations are given in Table S1a–d for Fig. 8 a–d, respectively. Pre-treatment of water samples are given as <0.2, <5.0, UNF, and AUT (for details see text) (DOC 435 kb)

ESM Fig. 2

NMS ordination plots of DGGE banding patterns after addition of leaf litter from a) Betula—Betula pendula, b) Fagus—Fagus silvatica, c) Pinus—Pinus silvestris over a 28-day period. T 0 = time zero, d 7–28 = days of incubation, FL = free-living bacteria, PA = particle-associated bacteria. Pre-treatment of water samples are given as <0.2, <5.0, UNF, and AUT (for details see text) (DOC 85 kb)

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Hutalle-Schmelzer, K.M.L., Zwirnmann, E., Krüger, A. et al. Changes in Pelagic Bacteria Communities Due to Leaf Litter Addition. Microb Ecol 60, 462–475 (2010). https://doi.org/10.1007/s00248-010-9639-0

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