Skip to main content

Advertisement

Log in

The Combination of Different Carbon Sources Enhances Bacterial Growth Efficiency in Aquatic Ecosystems

  • Environmental Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

The dissolved organic carbon (DOC) pool is composed of several organic carbon compounds from different carbon sources. Each of these sources may support different bacterial growth rates, but few studies have specifically analyzed the effects of the combination of different carbon sources on bacterial metabolism. In this study, we evaluated the response of several metabolic parameters, including bacterial biomass production (BP), bacterial respiration (BR), bacterial growth efficiency (BGE), and bacterial community structure, on the presence of three DOC sources alone and in combination. We hypothesized that the mixture of different DOC sources would increase the efficiency of carbon use by bacteria (BGE). We established a full-factorial substitutive design (seven treatments) in which the effects of the number and identity of DOC sources on bacterial metabolism were evaluated. We calculated the expected metabolic rates of the combined DOC treatments based on the single-DOC treatments and observed a positive interaction on BP, a negative interaction on BR, and, consequently, a positive interaction on BGE for the combinations. The bacterial community composition appeared to have a minor impact on differences in bacterial metabolism among the treatments. Our data indicate that mixtures of DOC sources result in a more efficient biological use of carbon. This study provides strong evidence that the mixture of different DOC sources is a key factor affecting the role of bacteria in the carbon flux of aquatic ecosystems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Explore related subjects

Discover the latest articles, news and stories from top researchers in related subjects.

References

  1. Kortelainen P (1999) Occurrence of humic waters. Temporal and spatial variability. In: Keskitalo J, Eloranta P (eds) Limnology of humic waters. Leiden, The Netherlands, pp 46–55

    Google Scholar 

  2. Chróst RJ (1990) Microbial ectoenzymes in aquatic environments. In: Overbeck J, Chróst RJ (eds) Aquatic microbial ecology. Springer-Verlag, New York, pp 47–78

    Chapter  Google Scholar 

  3. del Giorgio PA, Cole JJ (1998) Bacterial growth efficiency in natural aquatic systems. Annu Rev Ecol Systemat 29:503–541

    Article  Google Scholar 

  4. Amado AM, Meirelles-Pereira F, Vidal LDO, Sarmento H, Suhett A, Farjalla VF, Cotner J, Roland F (2013) Tropical freshwater ecosystems have lower bacterial growth efficiency than temperate ones. Front Microbiol 4:167

    PubMed Central  PubMed  Google Scholar 

  5. Amon RMW, Benner R (1996) Bacterial utilization of different size classes of dissolved organic matter. Limnol Oceanogr 41:41–51

    Article  CAS  Google Scholar 

  6. Berggren M, Laudon H, Jonsson A, Jansson M (2010) Nutrients constraints on metabolism affect the temperature regulation of aquatic bacterial growth efficiency. Microb Ecol 60:894–902

    Article  CAS  PubMed  Google Scholar 

  7. Biddanda B, Ogdahl M, Cotner J (2001) Dominance of bacterial metabolism in oligotrophic relative to eutrophic waters. Limnol Oceanogr 46:730–739

    Article  Google Scholar 

  8. 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 

  9. Farjalla VF, Esteves FA, Bozelli RL, Roland F (2002) Nutrient limitation of bacterial production in clear water Amazonian ecosystems. Hydrobiologia 489:197–205

    Article  CAS  Google Scholar 

  10. Farjalla VF, Faria BM, Esteves FA (2002) The relationship between DOC and planktonic bacteria in tropical coastal lagoons. Arch Hydrobiol 156:97–119

    Article  Google Scholar 

  11. Hall EK, Neuhauser C, Cotner JB (2008) Toward a mechanistic understanding of how natural bacterial communities respond to changes in temperature in aquatic ecosystems. Isme J 2:471–481

    Article  CAS  PubMed  Google Scholar 

  12. Hunt AP, Parry JD, Hamilton-Taylor J (2000) Further evidence of elemental composition as an indicator of the bioavailability of humic substances to bacteria. Limnol Oceanogr 45:237–241

    Article  CAS  Google Scholar 

  13. Weiss M, Simon M (1999) Consumption of labile dissolved organic matter by limnetic bacterioplankton: the relative significance of amino acids and carbohydrates. Aquat Microb Ecol 17:1–12

    Article  Google Scholar 

  14. 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 

  15. Kritzberg ES, Cole JJ, Pace MM, Granéli W (2005) Does autochthonous primary production drive variability in bacterial metabolism and growth efficiency in lakes dominated by terrestrial C inputs? Aquat Microb Ecol 38:103–111

    Article  Google Scholar 

  16. Roland F, Lobao LM, Vidal LO, Jeppesen E, Paranhos R, Huszar VLM (2010) Relationships between pelagic bacteria and phytoplankton abundances in contrasting tropical freshwaters. Aquat Microb Ecol 60:261–272

    Article  Google Scholar 

  17. Farjalla VF, Azevedo DA, Esteves FA, Bozelli RL, Roland F, Enrich-Prast A (2006) Influence of hydrological pulse on bacterial growth and DOC uptake in a clear-water Amazonian lake. Microb Ecol 52:334–344

    Article  PubMed  Google Scholar 

  18. Orwin KH, Wardle DA, Greenfield LG (2006) Context-dependent changes in the resistance and resilience of soil microbes to an experimental disturbance for three primary plant chronosequences. Oikos 112:196–208

    Article  Google Scholar 

  19. Loreau M (1998) Separating sampling and other effects in biodiversity experiments. Oikos 82:600–602

    Article  Google Scholar 

  20. Loreau M (2001) Microbial diversity, producer–decomposer interactions and ecosystem processes: a theoretical model. Proc Roy Soc Lond B Biol Sci 268:303–309

    Article  CAS  Google Scholar 

  21. Findlay S, Sinsabaugh R (2003) Aquatic ecosystems: interactivity of dissolved organic matter. Academic Press, Elsevier Science, USA

    Google Scholar 

  22. Farjalla VF, Marinho CC, Faria BM, Amado AM, Esteves FD, Bozelli RL, Giroldo D (2009) Synergy of fresh and accumulated organic matter to bacterial growth. Microb Ecol 57:657–666

    Article  CAS  PubMed  Google Scholar 

  23. Kankaala P, Peura S, Nykänen H, Sonninen E, Taipale S, Tiirola M, Jones R (2010) Impacts of added dissolved organic carbon on boreal freshwater pelagic metabolism and food webs in mesocosm experiments. Fundam Appl Limnol, Arch Hydrobiol 177:161–176

    Article  CAS  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  25. Suhett AL, MacCord F, Amado AM, Farjalla VF, Esteves FA (2004) Photodegradation of dissolved organic carbon in humic coastal lagoons (RJ, Brazil). In: Martin-Neto L (ed.) XII International meeting of International humic substances society, São Pedro, SP.

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

    Article  CAS  Google Scholar 

  27. Briand E, Pringault O, Jacquet S, Torreton J (2004) The use of oxygen microprobes to measure bacterial respiration for determining bacterioplankton growth efficiency. Limnol Oceanogr Meth 2:406–416

    Article  Google Scholar 

  28. Hobbie JE, Daley RJ, Jasper S (1977) Use of nuclepore filters for counting bacteria by fluorescence microscopy. Appl Environ Microbiol 33:1225–1228

    PubMed Central  CAS  PubMed  Google Scholar 

  29. Fry JC (1990) Direct methods and biomass estimation. Meth Microbiol 22:41–85

    Article  Google Scholar 

  30. Bratbak G (1985) Bacterial biovolume and biomass estimations. Appl Environ Microbiol 49:1488–1493

    PubMed Central  CAS  PubMed  Google Scholar 

  31. Muyzer G, Dewaal EC, Uitterlinden AG (1993) Profiling of complex microbial-populations by denaturing gradient gel-electrophoresis analysis of polymerase chain reaction-amplified genes-coding for 16S ribosomal-RNA. Appl Environ Microbiol 59:695–700

    PubMed Central  CAS  PubMed  Google Scholar 

  32. Loisel P, Harmand J, Zemb O, Latrille E, Lobry C, Delgenes JP, Godon J-P (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 

  33. Muyzer G, Smalla K (1998) Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie Leeuwenhoek 73:127–141

    Article  CAS  PubMed  Google Scholar 

  34. Farjalla VF, Srivastava DS, Marino NAC, Azevedo FD, Dib V, Lopes PM, Rosado AS, Bozelli RL, Esteves FA (2012) Ecological determinism increases with organism size. Ecology 93:1752–1759

    Article  PubMed  Google Scholar 

  35. Laque T, Farjalla VF, Rosado AS, Esteves FA (2010) Spatiotemporal variation of bacterial community composition and possible controlling factors in tropical shallow lagoons. Microb Ecol 59:819–829

    Article  PubMed  Google Scholar 

  36. Yu YH, Yan QY, Feng WS (2008) Spatiotemporal heterogeneity of plankton communities in Lake Donghu, China, as revealed by PCR-denaturing gradient gel electrophoresis and its relation to biotic and abiotic factors. FEMS Microbiol Ecol 63:328–337

    Article  CAS  PubMed  Google Scholar 

  37. Hardoim CCP, Costa R, Araújo FV, Hajdu E, Peixoto R, Lins U, Rosado AS, van Elsas JD (2009) Diversity of bacteria in the marine sponge Aplysina fulva in Brazilian coastal waters. Appl Environ Microbiol 75:3331–3343

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  38. Wardle DA, Bonner KI, Nicholson KS (1997) Biodiversity and plant litter: experimental evidence which does not support the view that enhanced species richness improves ecosystem function. Oikos 79:247–258

    Article  Google Scholar 

  39. Hector A (1998) The effect of diversity on productivity: detecting the role of species complementarity. Oikos 82:597–599

    Article  Google Scholar 

  40. Dang CK, Chauvet E, Gessner MO (2005) Magnitude and variability of process rates in fungal diversity–litter decomposition relationships. Ecol Lett 8:1129–1137

    Article  PubMed  Google Scholar 

  41. Findlay SEG, Sinsabaugh RL, Sobczak WV, Hoostal M (2003) Metabolic and structural response of hyporheic microbial communities to variations in supply of dissolved organic matter. Limnol Oceanogr 48:1608–1617

    Article  CAS  Google Scholar 

  42. Pinhassi J, Azam F, Hemphala J, Long RA, Martinez J, Zweifel UL, Hagstrom A (1999) Coupling between bacterioplankton species composition, population dynamics, and organic matter degradation. Aquat Microb Ecol 17:13–26

    Article  Google Scholar 

  43. Carlson CA, Giovannoni SJ, Hansell DA, Goldberg SJ, Parsons R, Otero MP, Vergin K, Wheeler BR (2002) Effect of nutrient amendments on bacterioplankton production, community structure, and DOC utilization in the northwestern Sargasso Sea. Aquat Microb Ecol 30:19–36

    Article  Google Scholar 

  44. Sinsabaugh RL, Findlay S, Franchini P, Fisher D (1997) Enzymatic analysis of riverine bacterioplankton production. Limnol Oceanogr 42:29–38

    Article  CAS  Google Scholar 

  45. Perdue EM (1998) Chemical composition, structure and metal binding properties. In: Hessen DO, Tranvik LJ (eds) Aquatic humic substances: ecology and biogeochemistry. Springer-Verlag, Berlin, pp 41–61

    Chapter  Google Scholar 

  46. Farjalla VF, Amado AM, Suhett AL, Meirelles-Pereira F (2009) DOC removal paradigms in highly humic aquatic ecosystems. Environ Sci Pollut Res 16:531–538

    Article  CAS  Google Scholar 

  47. Guenet B, Neill C, Bardoux G, Abbadie L (2010) Is there a linear relationship between priming effect intensity and the amount of organic matter input? Appl Soil Ecol 46:436–442

    Article  Google Scholar 

  48. De Haan H (1974) Effect of a fulvic acid fraction on the growth of a Pseudomonas from Tjeukemeer (The Netherlands). Freshwat Biol 4:301–310

    Article  Google Scholar 

  49. Eiler A, Langenheder S, Bertilsson S, Tranvik L (2003) Heterotrophic bacterial growth efficiency and community structure at different natural organic carbon concentrations. Appl Environ Microbiol 69:3701–3709

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  50. Sarmento H, Gasol JM (2012) Use of phytoplankton-derived dissolved organic carbon by different types of bacterioplankton. Environ Microbiol 14:2348–2360

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful to Petrobras, CAPES, CNPq, and FAPERJ for financial support and PhD scholarships. V.F. F. is particularly thankful to CNPq for a research productivity scholarship (Process 307490/2008-4) and F. M-P. to CAPES/FAPERJ PAPD Program (Proc.: E-26/102.567/2010). The authors also thank three anonymous reviewers and A.L. Suhett for valuable comments on this work and F.D. Azevedo and C.S. Haubrich for performing the molecular analyses.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to André M. Amado.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fonte, E.S., Amado, A.M., Meirelles-Pereira, F. et al. The Combination of Different Carbon Sources Enhances Bacterial Growth Efficiency in Aquatic Ecosystems. Microb Ecol 66, 871–878 (2013). https://doi.org/10.1007/s00248-013-0277-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-013-0277-1

Keywords

Navigation