Abstract
Dynamics of fluorescent dissolved organic matter (FDOM) in ocean environments has received attention over the past few decades. Although it has appeared that in situ production of oceanic FDOM is mainly due to bacteria, the production and bio- and photodegradation processes of bacterial FDOM have not been elucidated. In this study, a culture experiment with bacteria was carried out to assess the production and biodegradation processes of bacterial FDOM. Photodegradation of bacterial FDOM and dissolved organic carbon (DOC) was also examined by exposure to a solar simulator. Bacterial FDOM consists of six components which were determined by parallel factor analysis (PARAFAC). Fluorescence intensities of protein-like FDOM increased with the bacterial biomass, but the increases of humic-like FDOM lagged behind the protein-like FDOM by 5–10 days. Exposure to simulated sunlight caused significant decreases in fluorescence intensities of all components; 52–94% of the initial intensities were lost during 24 h. While, the DOC concentration exhibited a small decrease through the experiment (1.9–11.1%). These results showed that photodegradability of bacteria derived DOC was much less than the fluorescence, indicating that the lifetime of bacteria-derived DOC is much longer than the length estimated by the fluorescence. The role of photobleached FDOM derived from bacteria may be significant in the biogeochemical cycle at the surface layer.
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Aristegui J, Agustí S, Middelburg JJ, Duarte CM (2005) Respiration in the mesopelagic and bathypelagic zones of the oceans. In: del Giorgio PA, Williams PJB (eds) Respiration in aquatic ecosystems. Oxford University Press, Oxford, pp 147–180
Azam F, Malfatti F (2007) Microbial structuring of marine ecosystems. Nature 437:249–355
Blanchet M, Pringault O, Bouvy M, Catala P, Oriol L, Caparros J, Ortega-Retuerta E, Intertaglia L, West N, Agis M, Got P, Joux F (2015) Changes in bacterial community metabolism and composition during the degradation of dissolved organic matter from the jellyfish Aurelia aurita in a Mediterranean coastal lagoon. Environ Sci Pollut Res 22:13638–13653
Blunt JW, Copp BR, Keyzers RA, Munro MHG, Prinsep MR (2013) Marine natural products. Nat Prod Rep 30:237–323
Brophy JE, Carlson DJ (1989) Production of biologically refractory dissolved organic carbon by natural seawater microbial populations. Deep Sea Res 35:497–507
Calvet A, Li B, Ryder AG (2014) A rapid fluorescence based method for the quantitative analysis of cell culture media photo-degradation. Anal Chim Acta 807:111–119
Carlson CA, Hansell DA (2015) DOM sources, sinks, reactivity, and budgets. In: Hansell DA, Carlson CA (eds) Biogeochemistry of marine dissolved organic matter, 2nd edn. Academic, London, pp 66–126
Catalá TS, Reche I, Fuentes-Lema A, Romera-Castillo C et al (2015) Turnover time of fluorescent dissolved organic matter in the dark global ocean. Nat Commun. doi:10.1038/ncomms6986
Coble PG (1996) Characterization of marine and terrestrial DOM in seawater using excitation-emission matrix spectroscopy. Mar Chem 51:325–346
Coble PG, Spencer RGM, Baker A, Reynolds DM (2014) Aquatic organic matter fluorescence. In: Coble PG, Lead J, Baker A, Reynolds DM, Spencer RGM (eds) Aquatic organic matter fluorescence. Cambridge University Press, Yew York, pp 75–122
Cory RM, McKnight DM (2005) Fluorescence spectroscopy reveals ubiquitous presence of oxidized and reduced quinones in dissolved organic matter. Environ Sci Technol 39:8142–8149
del Giorgio PA, Cole JJ (1998) Bacterial growth efficiency in natural aquatic system. Annu Rev Ecol Syst 29:503–541
del Giorgio PA, Duarte CM (2002) Respiration in the open ocean. Nature 420:379–384
Dinasquet J, Kragh T, Schrøter M-L, Søndergaard M, Riemann L (2013) Functional and compositional succession of bacterioplankton in response to a gradient in bioavailable dissolved organic carbon. Environ Microbiol 15:2616–2628
Fellman JB, Hood E, Edwards RT, D’Amore DV (2009) Changes in the concentration, biodegradability, and fluorescent properties of dissolved organic matter during stormflows in coastal temperate watersheds. J Geophys Res Biogeosci 114:G01021. doi:10.1029/2008JG000790
Fellman JB, Hood E, Spencer RGM (2010) Fluorescence spectroscopy opens new windows into dissolved organic matter dynamics of freshwater ecosystems: a review. Limnol Oceanogr 55:2452–2462
Gasol JM, del Giorgio PA (2000) Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities. Sci Mar 64:197–224
Ghosh S, Leff LG (2013) Impacts of labile organic carbon concentration on organic and inorganic nitrogen utilization by a stream biofilm bacterial community. Appl Environ Microbiol 79:7130–7141
Goto S, Tada Y, Suzuki K, Yamashita Y (2017) Production and reutilization of fluorescent dissolved organic matter by a marine bacterial strain, Alteromonas macleodii. Front Microbiol 8:507. doi:10.3389/fmicb.2017.00507
Graneli W, Lindell MJ, Tranvik LJ (1996) Photooxidative CO2 production in lakes of different humic content. Limnol Oceanogr 41:698–706
Guo W, Yang L, Hong H, Stedmon CA et al (2011) Assessing the dynamics of chromophoric dissolved organic matter in a subtropical estuary using parallel factor analysis. Mar Chem 124:125–133
Hama T, Yanagi K, Hama J (2004) Decrease in molecular weight of photosynthetic products of marine phytoplankton during early diagenesis. Limnol Oceanogr 49:471–481
Hayase K, Shinozuka N (1995) Vertical distribution of fluorescent organic matter along with AOU and nutrients in the equatorial Central Pacific. Mar Chem 48:283–290
Helms JR, Stubbins A, Perdue EM, Green NW et al (2013) Photochemical bleaching of oceanic dissolved organic matter and its effect on absorption spectral slope and fluorescence. Mar Chem 155:81–91
Jiao N, Herndl GJ, Hansell DA, Benner R et al (2010) Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nat Rev Microbiol 8:593–599
Jørgensen L, Stedmon CA, Kragh T, Markager S et al (2011) Global trends in the fluorescence characteristics and distribution of marine dissolved organic matter. Mar Chem 126:139–148
Kawasaki N, Benner R (2006) Bacterial release of dissolved organic matter during cell growth and decline: molecular origin and composition. Limnol Oceanogr 51:2170–2180
Kitayama K, Hama T, Yanagi K (2007) Bioreactivity of peptidoglycan in seawater. Aquat Microb Ecol 46:85–93
Kowalczuk P, Cooper WJ, Whitehead PF, Durako MJ, Sheldon W (2003) Characterization of CDOM in an organic-rich river and surrounding coastal ocean in the South Atlantic Bight. Aquat Sci 65:384–401
Kowalczuk P, Durako MJ, Young H, Kahn AE, Cooper WJ, Gonsior M (2009) Characterization of dissolved organic matter fluorescence in the South Atlantic Bight with use of PARAFAC model: interannual variability. Mar Chem 113:182–196
Kramer GD, Herndl GJ (2004) Photo- and bioreactivity of chromophoric dissolved organic matter produced by marine bacterioplankton. Aquat Microb Ecol 36:239–246
Lapierre JF, del Giorgio PA (2014) Partial coupling and differential regulation of biologically and photochemically labile dissolved organic carbon across boreal aquatic networks. Biogeosciences 11:5969–5985
Lawaetz AJ, Stedmon CA (2009) Fluorescence intensity calibration using the Raman scatter peak of water. Appl Spectrosc 63:936–940
Lechtenfeld OJ, Hertkorn N, Shen Y, Witt M, Benner R (2015) Marine sequestration of carbon in bacterial metabolites. Nat Commun. doi:10.1038/ncomms7711
Lønborg C, Álvarez-Salgado XA, Davidson K, Miller AEJ (2009) Production of bioavailable and refractory dissolved organic matter by coastal heterotrophic microbial populations. Estuar Coast Shelf Sci 82:682–688
Middelboe M, Jørgensen NOG (2006) Viral lysis of bacteria: an important source of dissolved amino acids and cell wall compounds. J Mar Biol Assoc UK 86:605–612
Miller MP, McKnight DM, Chapra SC, Williams MW (2009) A model of degradation and production of three pools of dissolved organic matter in an alpine lake. Limnol Oceanogr 54:2213–2227
Mopper K, Kieber DJ, Stubbins A (2015) Marine photochemistry of organic matter: processes and impacts. In: Hansel DA, Carlson CA (eds) Biogeochemistry of marine dissolved organic matter. Academic, London, pp 389–450
Mostofa KMG, Liu-C-Q Yoshioka T, Vione D, Zhang Y, Sakugawa H (2013) Fluorescent dissolved organic matter in natural waters. In: Mostofa KMG, Yoshioka T, Mottaleb A, Vione D (eds) Photobiogeochemistry of organic matter. Springer, Berlin, pp 429–559
Murphy KR, Stedmon CA, Waite TD, Ruiz GM (2008) Distinguishing between terrestrial and autochthonous organic matter sources in marine environments using fluorescence spectroscopy. Mar Chem 108:40–58
Obernosterer I, Benner R (2004) Competition between biological and photochemical processes in the mineralization of dissolved organic carbon. Limnol Oceanogr 49:117–124
Obernosterer I, Ruardij P, Herndl GJ (2001) Spatial and diurnal dynamics of dissolved organic matter (DM) fluorescence and H2O2 and the photochemical oxygen demand of surface water DOM across the subtropical Atlantic Ocean. Limnol Oceanogr 46:632–643
Ogawa H, Amagai Y, Koike I, Kaiser K, Benner R (2001) Production of refractory dissolved organic matter by bacteria. Science 292:917–920
Omori Y, Hama T, Ishii M, Saito S (2010) Relationship between the seasonal change in fluorescent dissolved organic matter and mixed layer depth in the subtropical western North Pacific. J Geophys Res 115:C06001
Omori Y, Hama T, Ishii S, Saito S (2011) Vertical change in the composition of marine humic-like fluorescent dissolved organic matter in the subtropical western North Pacific and its relation to photoreactivity. Mar Chem 124:38–47
Omori Y, Hama T, Ishii M (2015) Photochemical bleaching of fluorescent dissolved organic matter in the subtropical North Pacific Ocean. Geochem J 49:175–184
Ridgwell A, Arndt S (2015) Why dissolved organics matter; DOC in ancient oceans and past climate change. In: Hansell DA, Carlson CA (eds) Biogeochemistry of marine dissolved organic matter, 2nd edn. Academic, London, pp 1–20
Santín C, Yamashita Y, Otero XL, Álvarez MÁ, Jaffé R (2009) Characterizing humic substances from estuarine soils and sediments by excitation-emission matrix spectroscopy and parallel factor analysis. Biogeochemistry 96:131–147
Shimotori K, Omori Y, Hama T (2009) Bacterial production of marine humic-like fluorescent dissolved organic matter and its biogeochemical importance. Aquat Microb Ecol 58:55–66
Shimotori K, Watanabe K, Hama T (2012) Fluorescence characteristics of humic-like fluorescent dissolved organic matter produced by various taxa of marine bacteria. Aquat Microb Ecol 65:249–260
Sipler RA, Bronk DA (2015) Dynamics of dissolved organic nitrogen. In: Hansell DA, Carlson CA (eds) Biogeochemistry of marine dissolved organic matter, 2nd edn. Academic, London, pp 128–232
Stedmon CA, Bro R (2008) Characterizing dissolved organic matter fluorescence with parallel factor analysis: a tutorial. Limnol Oceanogr Methods 6:572–579
Stedmon CA, Cory RM (2014) Biological origins and fate of fluorescent dissolved organic matter in aquatic environments. In: Coble PG, Lead J, Baker A, Reynolds DM, Spencer RG (eds) Aquatic organic matter fluorescence. Cambridge University Press, New York, pp 278–299
Stedmon CA, Markager S (2005a) Resolving the variability in dissolved organic matter fluorescence in temperate estuary and its catchment using PARAFAC analysis. Limnol Oceanogr 50:686–697
Stedmon CA, Markager S (2005b) Tracing the production and degradation of autochthonous fractions of dissolved organic matter by fluorescence analysis. Limnol Oceanogr 50:1415–1426
Stedmon CA, Nelson NB (2015) The optical properties of DOM in the ocean. In: Hansell DA, Carlson CA (eds) Biogeochemistry of marine dissolved organic matter, 2nd edn. Academic, London, pp 481–508
Stedmon CA, Markager S, Bro R (2003) Tracing dissolved organic matter in aquatic environments using a new approach to fluorescence spectroscopy. Mar Chem 82:239–254
Stubbins A, Dittmar T (2015) Illuminating the deep: molecular signatures of photochemical alteration of dissolved organic matter from North Atlantic Deep Water. Mar Chem 177:318–324
Stubbins A, Spencer RGM, Chen H, Hatcher PG, Mopper K, Hernes PJ, Mwamba VL, Mangangu AM, Wabakanghanzi JN, Six J (2010) Illuminated darkness: molecular signatures of Congo River dissolved organic matter and its photochemical alteration as revealed by ultrahigh precision mass spectrometry. Limnol Oceanogr 55:1467–1477
Stubbins A, Niggemann J, Dittmar T (2012) Photo-lability of deep ocean dissolved black carbon. Biogeosciences 9:1661–1670
Timko SA, Maydanov A, Pittelli SL, Conte MH, Cooper WJ, Koch BP, Schmitt-Kopplin P, Gonsior M (2015) Front Mar Sci 2:66. doi:10.3389/fmars.2015.00066
Wear EK, Koepfler ET, Smith EM (2014) Spatiotemporal variability in dissolved organic matter composition is more strongly related to bacterioplankton community composition than to metabolic capability in blackwater estuarine system. Estuar Coast 37:119–133
Wear EK, Carlson CA, James AK, Brzezinski MA, Windecker LA, Nelson CE (2015) Synchronous shifts in dissolved organic carbon bioavailability and bacterial community responses over the course of an upwelling-driven phytoplankton bloom. Limnol Oceanogr 60:657–677
Yamashita Y, Tanoue E (2003) Chemical characterization of protein-like fluorophores in DOM in relation to aromatic amino acids. Mar Chem 82:255–271
Yamashita Y, Jaffé R, Maie N, Tanoue E (2008) Assessing the dynamics of dissolved organic matter (DOM) in coastal environments by excitation emission matrix fluorescence and parallel factor analysis (EEM-PARAFAC). Limnol Oceanogr 53:1900–1908
Yamashita T, Cory RM, Nishioka J, Kuma K, Tanoue E, Jaffé R (2010) Fluorescence characteristics of dissolved organic matter in the deep waters of the Okhotsk Sea and the northwestern North Pacific Ocean. Deep-Sea Res II 57:1478–1485
Acknowledgements
We thank the Chemical Analysis Division, Research Facility Center for Science and Technology, University of Tsukuba, for the use of their spectrofluorometer. This work was supported by Japan Society for the Promotion of Science KAKENHI Grant Numbers 15K13599 and 16H02967.
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Arai, K., Wada, S., Shimotori, K. et al. Production and degradation of fluorescent dissolved organic matter derived from bacteria. J Oceanogr 74, 39–52 (2018). https://doi.org/10.1007/s10872-017-0436-y
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DOI: https://doi.org/10.1007/s10872-017-0436-y