Skip to main content

Advertisement

Log in

Influence of water mixing on the inhibitory effect of UV radiation on primary and bacterial production in Mediterranean coastal water

  • Research Article
  • Published:
Aquatic Sciences Aims and scope Submit manuscript

Abstract

The scaling of the solar ultraviolet radiation (UVR, 280–400 nm) effect on phyto- and bacterio-plankton at the ecosystem level is difficult since its estimate is often based on short-time incubation experiments performed at fixed depths, neglecting the previous days’ radiation history and the variable radiation caused by vertical mixing. To examine this issue, we measured primary (PP) and bacterial (BP) production in samples from coastal water in the Northwest Mediterranean Sea incubated at fixed depths or moving vertically within the water column (0–8 m) with a periodicity of 22 min, exposed to full sun, PAR or maintained in dark. Three experiments were carried out on consecutive days to measure day-to-day variations in planktonic response. In surface waters, PP was inhibited by ~32 to 42% by UVR, and BP was inhibited by ~50 to 70% by solar radiation (UVR + PAR). We observed a general decrease in the integrated inhibition of PP due to UVR for both fixed and moving incubations over the 3 days from ~27% of inhibition to non-significant inhibition. In contrast, large discrepancies were observed in the integrated inhibition of BP due to solar radiation (UVR + PAR) between fixed and moving incubations. Whereas both type of incubations gave similar estimation of solar radiation inhibition on day 1 (~25%), inhibition became much higher for fixed incubation compared to moving incubation on days 2 and 3. Differences in responses between days suggest that light history, spectral quality, photoadaptation or acclimation may be important factors in daily observed responses. Our results also underline, for the first time, the importance of the vertical mixing in the BP inhibition by solar radiation.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aas P, Lyons MM, Pledger R, Mitchell DL, Jeffrey WH (1996) Inhibition of bacterial activities by solar radiation in nearshore waters and the Gulf of Mexico. Aquat Microb Ecol 11:229–238

    Article  Google Scholar 

  • Abboudi M, Jeffrey WH, Ghiglione J-F, Pujo-Pay M, Oriol L, Sempéré R, Charrière B, Joux F (2008) 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 55:344–357

    Article  PubMed  CAS  Google Scholar 

  • Alonso-Saez L, Gasol JM, Lefort T, Hofer J, Sommaruga R (2006) Effect of natural sunlight on bacterial activity and differential sensitivity of natural bacterioplankton groups in northwestern Mediterranean coastal waters. Appl Environ Microbiol 72:5806–5813

    Article  PubMed  CAS  Google Scholar 

  • Banaszak AT (2003) Photoreactive physiological and biochemical responses of aquatic organisms. In: Helbling EW, Zagarese HE (eds) UV effects in aquatic organisms and ecosystems. The Royal Society of Chemistry, Cambridge, pp 329–356

    Chapter  Google Scholar 

  • Bancroft BA, Baker NJ, Blaustein AR (2007) Effects of UVB radiation on marine and freshwater organisms: a synthesis through meta-analysis. Ecol Lett 10:332–345

    Article  PubMed  Google Scholar 

  • Barbieri ES, Villafañe VE, Helbling EW (2002) Experimental assessment of UVR effects on temperate marine phytoplankton when exposed to variable radiation regimes. Limnol Oceanogr 47:1648–1655

    Article  Google Scholar 

  • Berney M, Weilenmann H-U, Egli T (2007) Adaptation to UVA radiation of E coli growing in continuous culture. J Photochem Photobiol B Biol 86:149–159

    Article  CAS  Google Scholar 

  • Bertoni R, Balseiro E (2005) Mixing layer running incubator (MIRI): an instrument for incubating samples while moving vertically in the mixing layer. Limnol Oceanogr Methods 3:158–163

    Article  Google Scholar 

  • Booth MG, Hutchinson L, Brumsted M, Aas P, Coffin RB, Downer RC, Kelley CA, Lyons MM, Pakulski JD, Sandvik SLH, Jeffrey WH, Miller RV (2001) Quantification of recA expression as an indicator of repair potential in marine bacterioplankton communities of Antarctica. Aquat Microb Ecol 24:51–59

    Article  Google Scholar 

  • Bullock AK, Jeffrey WH (2010) Temperature and solar radiation interactions on 3H-leucine incorporation by bacterioplankton in a subtropical estuary. Photochem Photobiol 86:593–599

    Article  PubMed  CAS  Google Scholar 

  • Cauwet G (1994) HTCO method for dissolved organic carbon analysis in seawater: influence of catalyst on blank estimation. Mar Chem 47:55–64

    Article  CAS  Google Scholar 

  • Church MJ, Ducklow HW, Karl DM (2004) Light dependence of [3H] leucine incorporation in the oligotrophic North Pacific Ocean. Appl Environ Microbiol 70:4079–4087

    Article  PubMed  CAS  Google Scholar 

  • Conan P, Joux F, Torréton J-P, Pujo-Pay M, Douki T, Rochelle-Newall E, Mari X (2008) Effect of solar ultraviolet radiation on bacterio- and phytoplankton activity in a large coral reef lagoon (SW New Caledonia). Aquat Microb Ecol 52:83–98

    Article  Google Scholar 

  • Fitzwater SE, Knauer GA, Martin JH (1982) Metal contamination and primary production: field and laboratory methods of control. Limnol Oceanogr 27:544–551

    Article  CAS  Google Scholar 

  • Friedberg EC (2003) DNA damage and repair. Nature 421:436–440

    Article  PubMed  Google Scholar 

  • Gao G, Gao K, Giordano M (2009) Responses to solar UV radiation of the diatom Skeletonema costatum (Bacillariophyceae) grown at different Zn2+ concentrations. J Phycol 45:119–129

    Article  CAS  Google Scholar 

  • Häder D-P, Kumar HD, Smith RC, Worrest RC (2007) Effects of solar UV radiation on aquatic ecosystems and interactions with climate change. Photochem Photobiol 6:267–285

    Article  Google Scholar 

  • Heraud P, Roberts S, Shelly K, Beardall J (2005) Interactions between UV-B exposure and phosphorus nutrition. II. Effects on rates of damage and repair. J Phycol 41:1212–1218

    Article  CAS  Google Scholar 

  • Huot Y, Jeffrey WH, Davis RF, Cullen JJ (2000) Damage to DNA in bacterioplankton: a model of damage by ultraviolet radiation and its repair as influenced by vertical mixing. Photochem Photobiol 72:62–74

    Article  PubMed  CAS  Google Scholar 

  • Jeffrey WH, Pledger RJ, Aas P, Hager S, Coffin RB, Von Haven R, Mitchell DL (1996) Diel and depth profiles of DNA photodamage in bacterioplankton exposed to ambient solar ultraviolet radiation. Mar Ecol Prog Ser 137:283–291

    Article  CAS  Google Scholar 

  • Jiao N, Zhang Y, Zeng Y, Hong N, Liu R, Chen F, Wang P (2007) Distinct distribution pattern of abundance and diversity of aerobic anoxygenic phototrophic bacteria in the global ocean. Environ Microbiol 9:3091–3099

    Article  PubMed  CAS  Google Scholar 

  • Joint I, Jordan MB (2008) Effect of short-term exposure to UVA and UVB on potential phytoplankton production in UK coastal waters. J Plankton Res 30:199–210

    Article  CAS  Google Scholar 

  • Joux F, Jeffrey WH, Lebaron P, Mitchell DL (1999) Marine bacterial isolates display diverse responses to UV-B radiation. Appl Environ Microbiol 65:3820–3827

    PubMed  CAS  Google Scholar 

  • Joux F, Jeffrey WH, Abboudi M, Pujo-Pay M, Oriol L, Neveux J, Naudin J-J (2009) Ultraviolet radiation in the Rhone lenses of low salinity and marine waters of the northwestern Mediterranean Sea: attenuation and effects on bacterial production and net community production. Photochem Photobiol 85:783–793

    Article  PubMed  CAS  Google Scholar 

  • Kirchman DL (1993) Leucine incorporation as a measure of biomass production by heterotrophic bacteria. In: Kemp PF (ed) Handbook of methods in aquatic microbial ecology. Lewis Publishers, Boca Raton, pp 509–512

    Google Scholar 

  • Köhler J, Schmitt M, Krumbeck H, Kapfer M, Litchman E, Neale PJ (2001) Effects of UV on carbon assimilation of phytoplankton in a mixed water column. Aquat Sci 63:294–309

    Article  Google Scholar 

  • Lami R, Zuzana Cuperová C, Ras J, Lebaron P, Koblízek M (2009) Distribution of free-living and particle-attached aerobic anoxygenic phototrophic bacteria in marine environments. Aquat Microb Ecol 55:31–38

    Article  Google Scholar 

  • Lizon F, Lagadeuc Y (1998) Comparisons of primary production values estimated from different incubation times in a coastal sea. J Plank Res 20:371–381

    Article  Google Scholar 

  • Lorenzen CJ (1967) Determination of chlorophyll and pheopigments: spectrometric equations. Limnol Oceanogr 12:343–346

    Article  CAS  Google Scholar 

  • Marcoval MA, Villafañe VE, Helbling EW (2008) Combined effects of solar ultraviolet radiation and nutrients addition on growth, biomass and taxonomic composition of coastal marine phytoplankton communities of Patagonia. J Photochem Photobiol 91:157–166

    Article  CAS  Google Scholar 

  • Modenutti BE, Balseiro EG, Callieri C, Bertoni R, Queimaliños CP (2005) Effect of UV-B and different PAR intensities on the primary production of the mixotrophic planktonic ciliate Stentor araucanus. Limnol Oceanogr 50:864–871

    Article  Google Scholar 

  • Morán XAG, Massana R, Gasol JM (2001) Light conditions affect the measurement of oceanic bacterial production via leucine uptake. Appl Environ Microbiol 67:3795–3801

    Article  PubMed  Google Scholar 

  • Morán XAG, Estrada M, Gasol JM, Pedrós-Alió C (2002) Dissolved primary production and the strength of phytoplankton–bacterioplankton coupling in contrasting marine regions. Microb Ecol 44:217–223

    Article  PubMed  Google Scholar 

  • Neale PJ (2001) Modeling the effects of ultraviolet radiation on estuarine phytoplankton production: impact of variations in exposure and sensitivity to inhibition. J Photochem Photobiol B Biol 62:1–8

    Article  CAS  Google Scholar 

  • Neale PJ, Helbling EW, Zagarese HE (2003) Modulation of UVR exposure and effects by vertical mixing and advection. In: Helbling EW, Zagarese HE (eds) UV effects in aquatic organisms and ecosystems. The Royal Society of Chemistry, Cambridge, pp 107–134

    Chapter  Google Scholar 

  • Pakulski JD, Baldwin A, Dean A, Durkin S, Karentz D, Kelley CA, Scott K, Spero HJ, Wilhelm S, Jeffrey WH (2007) Responses of heterotrophic bacteria to latitudinal variation in solar irradiance. Aquat Microb Ecol 47:153–162

    Article  CAS  Google Scholar 

  • Pausz C, Herndl GJ (1999) Role of ultraviolet radiation on phytoplankton extracellular release and its subsequent utilization by marine bacterioplankton. Aquat Microb Ecol 18:85–93

    Article  Google Scholar 

  • Platt T, Sathyendranath S (1993) The estimation of phytoplankton production in the ocean from chlorophyll and light data. J Geophys Res 8:14561–14576

    Article  Google Scholar 

  • Shiah FK, Chen TY, Gong GC, Chen CC, Chiang KP, Hung JJ (2001) Differential coupling of bacterial and primary production in mesotrophic and oligotrophic systems of the East China Sea. Aquat Microb Ecol 23:273–282

    Article  Google Scholar 

  • Smith DC, Azam F (1992) A simple, economical method for measuring bacterial protein synthesis rates in seawater using 3H-leucine. Mar Microb Food Webs 6:107–114

    Google Scholar 

  • Sommaruga R (2003) UVR and its effects on species interactions. In: Helbling EW, Zagarese HE (eds) UV effects in aquatic organisms and ecosystems. The Royal Society of Chemistry, Cambridge, pp 485–508

    Chapter  Google Scholar 

  • Steeman-Nielsen E (1952) The use of radioactive carbon for measuring organic production in the sea. J Cons Int Explor Mer 18:117–140

    Google Scholar 

  • Tréguer P, Le Corre P (1975) Manuel d’analyse des sels nutritifs dans l’eau de mer. Utilisation de l’Autoanalyzer II Technicon. 2nd édn. Laboratoire d’Océanographie chimique, Université de Bretagne Occidentale, Brest France

  • Van den Meersche K, Middelburg JJ, Soetaert K, van Rijswijk P, Boschker HTS, Heip CHR (2004) Carbon–nitrogen coupling and algal-bacterial interactions during an experimental bloom: modeling a 13C tracer experiment. Limnol Oceanogr 49:862–878

    Article  Google Scholar 

  • Villafañe VE, Andrade M, Lairana V, Zaratti F, Helbling EW (1999) Inhibition of phytoplankton photosynthesis by solar ultraviolet radiation: studies in Lake Titicaca, Bolivia. Freshw Biol 42:215–224

    Article  Google Scholar 

  • Villafañe VE, Helbling EW, Zagarase HE (2001) Solar ultraviolet radiation and its impact on aquatic systems of Patagonia, South America. Ambio 30:112–117

    PubMed  Google Scholar 

  • Visser PM, Poos JJ, Scheper BB, Boelen P, Van Duyl FC (2002) Diurnal variations in depth profiles of UV-induced DNA damage and inhibition of bacterioplankton production in tropical coastal waters. Mar Ecol Prog Ser 228:25–32

    Article  CAS  Google Scholar 

  • Wängberg S-Å, Andreasson KIM, Garde K, Gustavson K, Henriksen P, Reinthaler T (2006) Inhibition of primary production by UV-B radiation in an arctic bay—model calculations. Aquat Sci 68:117–128

    Article  Google Scholar 

  • Xenopoulos MA, Schindler DW (2003) Differential responses to UVR by bacterioplankton and phytoplankton from the surface and the base of the mixed layer. Freshw Biol 48:108–122

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank the crew of the Service d’Observation du Laboratoire Arago for their assistance during field sampling and incubation. We also acknowledge Météo France for the release of the wind speed data and E. Balseiro for revising the early version of the manuscript. This study was funded by the CNRS-PROOF program (“Induction of microbial community responses and dissolved organic matter transformation by UltraViolet radiation in marine ECOsystems” [UVECO] project) and by National Science Foundation Office of International Science and Engineering U.S-France Cooperative Science Program grant 0340764 to W.H.J.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fabien Joux.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Fig S1 (DOC 263 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bertoni, R., Jeffrey, W.H., Pujo-Pay, M. et al. Influence of water mixing on the inhibitory effect of UV radiation on primary and bacterial production in Mediterranean coastal water. Aquat Sci 73, 377–387 (2011). https://doi.org/10.1007/s00027-011-0185-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00027-011-0185-8

Keywords

Navigation