Skip to main content
Log in

Alteration of chromophoric dissolved organic matter by solar UV radiation causes rapid changes in bacterial community composition

  • Paper
  • Published:
Photochemical & Photobiological Sciences Aims and scope Submit manuscript

Abstract

We evaluated the effect of photochemical alterations of chromophoric dissolved organic matter (CDOM) on bacterial abundance, activity and community composition in a coastal lagoon of the Atlantic Ocean with high dissolved organic carbon concentration. On two occasions during the austral summer, bacteria-free water of the lagoon was exposed to different regions of the solar spectrum (full solar radiation, UV-A + PAR, PAR) or kept in the dark. Subsequently, dilution cultures were established with bacterioplankton from the lagoon that were incubated in the pre-exposed water for 5 h in the dark. Cell abundance, activity, and community composition of bacterioplankton were assessed before and after incubation in the different treatments. Changes in absorption, fluorescence, and DOC concentration were used as proxies for CDOM photoalteration. We found a significant CDOM photobleaching signal, DOC loss, as well as a stimulation of bacterial activity in the treatments pre-exposed to UV radiation, suggesting increased bioavailability of DOM. Bacterial community analysis by fluorescence in situ hybridization revealed that this stimulation was mainly accompanied by the specific enrichment of Alpha- and Betaproteobacteria. Thus, our results suggest that CDOM photoalteration not only stimulates bacterioplankton growth, but also induces rapid changes in bacterioplankton composition, which can be of relevance for ecosystem functioning, particularly considering present and future changes in the input of terrestrial CDOM to aquatic systems.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. C. L. Osburn and D. P. Morris, in Photochemistry of chromophoric dissolved organic matter in natural waters, in UV effects in aquatic organisms and ecosystems, ed. E. W. Helbling and H. Zagarese, The Royal Society of Chemistry, Cambridge, 2003, pp. 185–217.

  2. K. L. Bushaw, R. G. Zepp, M. A. Tarr, D. Schulz-Janders, R. A. Bourbonniere, R. E. Hodson, W. L. Miller, D. A. Bronk, M. A. Moran, Photochemical release of biologically available nitrogen from aquatic dissolved organic matter Nature 1996 381 404–407.

    Article  CAS  Google Scholar 

  3. W. L. Miller, M. A. Moran, Interaction of photochemical and microbial processes in the degradation of refractory dissolved organic matter from a coastal marine environment Limnol. Oceanogr. 1997 42 1317–1324.

    Article  CAS  Google Scholar 

  4. M. A. Moran, R. G. Zepp, Role of photoreactions in the formation of biologically labile compounds from dissolved organic matter Limnol. Oceanogr. 1997 42 1307–1316.

    Article  CAS  Google Scholar 

  5. B. A. Biddanda, J. B. Cotner, Enhancement of dissolved organic matter bioavailability by sunlight and its role in the carbon cycle of Lakes Superior and Michigan J. Great Lakes Res. 2003 29 228–241.

    Article  CAS  Google Scholar 

  6. R. G. Zepp, T. V. Callaghan, D. J. Erickson, Interactive effects of ozone depletion and climate change on biogeochemical cycles Photochem. Photobiol. Sci. 2003 2 51–61.

    Article  CAS  PubMed  Google Scholar 

  7. R. J. Kieber, X. Zhou, K. Mopper, Formation of carbonyl compounds from UV-induced photodegradation of humic substances in natural waters: Fate of riverine carbon to the sea Limnol. Oceanogr. 1990 35 1503–1515.

    Article  CAS  Google Scholar 

  8. K. Mopper and D. J. Kieber, Marine photochemistry and its impact on carbon cycling, in The effects of UV radiation in the marine environment, ed. S. Mora, S. Demers and M. Vernet, Cambridge University Press, Cambridge, 2000, pp. 101–129.

    Chapter  Google Scholar 

  9. M. J. Lindell, W. Granéli, L. J. Tranvik, Enhanced bacterial growth in response to photochemical transformation of dissolved organic matter Limnol. Oceanogr. 1995 40 195–199.

    Article  Google Scholar 

  10. R. G. Wetzel, P. G. Hatcher, T. S. Bianchi, Natural photolysis by ultraviolet irradiance of recalcitrant dissolved organic matter to simple substrates for rapid bacterial metabolism Limnol. Oceanogr. 1995 40 1369–1380.

    Article  CAS  Google Scholar 

  11. M. J. Lindell, W. Granéli, L. J. Tranvik, Impact of solar (UV)-radiation on bacterial growth in lakes Aquat. Microb. Ecol. 1996 11 135–141.

    Article  Google Scholar 

  12. N. O. G. Jørgensen, L. Tranvik, H. Edling, W. Granéli, M. Lindell, Effects of sunlight on occurrence and bacterial turnover of specific carbon and nitrogen compounds in lake water FEMS Microb. Ecol. 1998 25 217–227.

    Article  Google Scholar 

  13. S. Bertilsson, L. J. Tranvik, Photochemically produced carboxylic acids as substrates for freshwater bacterioplankton Limnol. Oceanogr. 1998 43 885–895.

    Article  CAS  Google Scholar 

  14. M. Pérez, R. Sommaruga, Interactive effects of solar radiation and dissolved organic matter on bacterial activity and community structure Environ. Microbiol. 2007 9 2200–2210.

    Article  PubMed  PubMed Central  Google Scholar 

  15. D. Conde, L. Aubriot, S. Bonilla, R. Sommaruga, Marine intrusions in a coastal lagoon enhance the negative effect of solar UV radiation on phytoplankton photosynthetic rates Mar. Ecol. Prog. Ser. 2002 240 57–70.

    Article  CAS  Google Scholar 

  16. C. A. Stedmon, S. Markager, H. Kaasb, Optical properties and signatures of chromophoric dissolved organic matter (CDOM) in Danish coastal waters Estuar. Coast. Shelf Sci. 2000 51 267–278.

    Article  CAS  Google Scholar 

  17. P. Kuhn, H. Brownman, B. McArthur, J. F. St-Pierre, Penetration of ultraviolet radiation in the waters of the estuary and Gulf of St. Lawrence Limnol. Oceanogr. 1999 44 710–716.

    Article  CAS  Google Scholar 

  18. D. Conde, L. Aubriot, R. Sommaruga, Changes in UV penetration associated with marine intrusions and freshwater discharge in a shallow coastal lagoon of the Southern Atlantic Ocean Mar. Ecol. Prog. Ser. 2000 207 19–31.

    Article  Google Scholar 

  19. I. Obernosterer, R. Sempéré, G. J. Herndl, Ultraviolet radiation induces reversal of the bioavailability of DOM to marine bacterioplankton Aquat. Microb. Ecol. 2001 24 61–68.

    Article  Google Scholar 

  20. M. A. Moran and J. S. Covert, Photochemically mediated linkages between dissolved organic matter and bacterioplankton, in Aquatic Ecosystems: Interactivity of Dissolved Organic Matter, ed. S. Findlay and R. Sinsabaugh, Academics Aquatic Ecology Series, 2003, pp. 244–262.

    Google Scholar 

  21. M. Abboudi, W. H. Jeffrey, J. F. Ghiglione, M. Pujo-Pay, L. Oriol, R. Sempéré, B. Charriere, F. Joux, Effects of photochemical transformations of dissolved organic matter on bacterial metabolism and diversity in three contrasting coastal sites in the Northwestern Mediterranean Sea during summer Microb. Ecol. 2008 55 344–357.

    Article  CAS  PubMed  Google Scholar 

  22. B. M. Fuchs, M. V. Zubkov, K. Sahm, P. H. Burkill, R. Amann, Changes in community composition during dilution cultures of marine bacterioplankton as assessed by flow cytometric and molecular biological techniques Environ. Microbiol. 2000 2 191–201.

    Article  CAS  PubMed  Google Scholar 

  23. C. Piccini, D. Conde, C. Alonso, R. Sommaruga, J. Pernthaler, Blooms of single bacterial species in a coastal lagoon of the southwestern Atlantic Ocean Appl. Environ. Microbiol. 2006 72 6560–6568.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. K. G. Porter, Y. S. Feig, The use of DAPI for identifying and counting aquatic microflora Limnol. Oceanogr. 1980 25 943–948.

    Article  Google Scholar 

  25. D. L. Kirchman and H. W. Ducklow, Estimating conversion factors for the thymidine and leucine methods for measuring bacterial production, in Handbook of methods in aquatic microbial ecology, ed. P. F. Kemp, B. F. Sherr, E. B. Sherr and J. Cole, Lewis Publishers, Boca Raton, Florida, 1993, pp. 513–517.

    Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. E. Teira, T. Reinthaler, A. Pernthaler, J. Pernthaler, G. J. Herndl, Combining catalyzed reporter deposition-fluorescence in situ hybridization and microautoradiography to detect substrate utilization by Bacteria and Archaea in the deep ocean Appl. Environ. Microbiol. 2004 70 4411–4414.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. A. Neef, Anwendung der in situ Einzelzell-Identifizierung von Bakterien zur Populationsanalyse in komplexen mikrobiellen Biozönosen, PhD thesis. Technische Universität München, 1997.

    Google Scholar 

  29. W. Manz, R. Amann, W. Ludwig, M. Wagner, K. H. Schleifer, Phylogenetic oligodeoxynucleotide probes for the major subclasses of Proteobacteria: Problems and solutions Syst. Appl. Microbiol. 1992 15 593–600.

    Article  Google Scholar 

  30. W. Manz, R. Amann, W. Ludwig, M. Vancanneyt, K. H. Schleifer, Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum cytophaga-flavobacter-bacteroides in the natural environment Microbiology 1996 142 1097–1106.

    Article  CAS  PubMed  Google Scholar 

  31. C. Roller, M. Wagner, R. Amann, W. Ludwig, K. H. Schleifer, Probing of Gram-positive bacteria with high DNA G + C content using 23S rRNA-targeted oligonucleotides Microbiology 1994 140 2849–2858.

    Article  CAS  PubMed  Google Scholar 

  32. H. Daims, A. Bruhl, R. Amann, K. H. Schleifer, M. Wagner, 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. 1999 22 434–444.

    Article  CAS  PubMed  Google Scholar 

  33. J. Pernthaler, A. Pernthaler, R. Amann, Automated enumeration of groups of marine picoplankton after fluorescence in situ hybridization Appl. Environ. Microbiol. 2003 69 2631–2637.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. D. J. Kieber, J. McDaniel, K. Mopper, Photochemical source of biological substrates in seawater: implications for carbon cycling Nature 1989 341 637–639.

    Article  CAS  Google Scholar 

  35. I. Reche, M. L. Pace, J. Cole, Modeled effects of dissolved organic carbon and solar spectra on photobleaching in lake ecosystems Ecosystems 2000 3 419–432.

    Article  CAS  Google Scholar 

  36. D. L. Kirchman, H. W. Ducklow, R. Mitchell, Estimates of bacterial growth from changes in uptake rates and biomass Appl. Environ. Microbiol. 1982 44 1296–1307.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. J. W. Ammermann, J. A. Fuhrman, A. Hagström, F. Azam, Bacterioplankton growth in seawater: I. Growth, kinetics and cellular characteristics in seawater cultures Mar. Ecol. Prog. Ser. 1984 18 31–39.

    Article  Google Scholar 

  38. S. L. McCallister, J. E. Bauer, J. Kelly, H. W. Ducklow, Effects of sunlight on decomposition of estuarine dissolved organic C, N and P and bacterial metabolism Aquat. Microb. Ecol. 2005 40 25–35.

    Article  Google Scholar 

  39. A. Pernthaler, J. Pernthaler, H. Eilers, R. Amann, Growth patterns of two marine isolates: adaptations to substrate patchiness? Appl. Environ. Microbiol. 2001 67 4077–4083.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. F. Schut, R. A. Prins, J. C. Gottschal, Oligotrophy and pelagic marine bacteria: facts and fiction Aquat. Microb. Ecol. 1997 12 177–202.

    Article  Google Scholar 

  41. J. Pinhassi, A. Hagström, Seasonal succession in marine bacterioplankton Aquat. Microb. Ecol. 2000 21 245–256.

    Article  Google Scholar 

  42. M. Simon, F. Azam, Protein content and protein synthesis rates of planktonic marine bacteria Mar. Ecol. Prog. Ser. 1989 51 201–213.

    Article  CAS  Google Scholar 

  43. K. Flõrdh, P. S. Cohen, S. Kjelleberg, Ribosomes exist in large excess over the apparent demand for protein synthesis during carbon starvation in marine Vibrio sp. strain CCUG 15956 J. Bacteriol. 1992 174 6780–6788.

    Article  Google Scholar 

  44. J. M. Gasol, X. A. G. Morán, Effects of filtration on bacterial activity and picoplankton community structure as assessed by flow cytometry Aquat. Microb. Ecol. 1999 16 251–264.

    Article  Google Scholar 

  45. E. B. Sherr, B. F. Sherr, C. T. Sigmon, Activity of marine bacteria under incubated and in situ conditions Aquat. Microb. Ecol. 1999 20 213–223.

    Article  Google Scholar 

  46. M. T. Suzuki, Effect of protistan bacterivory on coastal bacterioplankton diversity Aquat. Microb. Ecol. 1999 20 261–272.

    Article  Google Scholar 

  47. H. Schõfer, P. Servais, G. Muyzer, Successional changes in the genetic diversity of a marine assemblage during confinement Arch. Mikrobiol. 2000 173 138–145.

    Article  Google Scholar 

  48. H. Schäfer, L. Bernard, C. Courties, P. Lebaron, P. Servais, R. Pukall, E. Stackebrandt, M. Troussellier, T. Guindulain, J. Vives-Rego, G. Muyzer, Microbial community dynamics in Mediterranean nutrient-enriched seawater mesocosms: changes in the genetic diversity of bacterial populations FEMS Microbiol. Ecol. 2001 34 243–253.

    Article  PubMed  Google Scholar 

  49. H. Eilers, J. Pernthaler, F. O. Glöckner, R. Amann, Culturability and in situ abundance of pelagic bacteria from the North Sea Appl. Environ. Microbiol. 2000 66 3044–3051.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. R. Massana, C. Pedrós-Alió, E. O. Casamayor, J. M. Gasol, Changes in marine bacterioplankton phylogenetic composition during incubations designed to measure biogeochemically significant parameters Limnol. Oceanogr. 2001 46 1181–1188.

    Article  Google Scholar 

  51. L. Giuliano, E. De Domenico, M. G. Höfle, M. M. Yakimov, Identification of culturable oligotrophic bacteria within naturally occurring bacterioplankton communities of the Ligurian Sea by 16S rRNA sequencing and probing Microb. Ecol. 1999 37 77–85.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ruben Sommaruga.

Additional information

This article was published as part of the themed issue on “Environmental effects of UV radiation”.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Piccini, C., Conde, D., Pernthaler, J. et al. Alteration of chromophoric dissolved organic matter by solar UV radiation causes rapid changes in bacterial community composition. Photochem Photobiol Sci 8, 1321–1328 (2009). https://doi.org/10.1039/b905040j

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1039/b905040j

Navigation