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Photo-biochemical transformation of dissolved organic matter on the surface of the coastal East Antarctic ice sheet

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Abstract

Recent studies have highlighted the composition and complexity of dissolved organic matter (DOM) in glacial environments. Climate-induced changes to glacier runoff are projected to be an important source of DOM to coastal ecosystems. Photochemical and microbial (termed photo-biochemical) degradation of DOM would determine its fate on the glacier surface and in recipient coastal ecosystems. In order to understand the molecular imprints of photo-biochemical alteration of DOM, in situ field experiments were conducted over a period of 35 days in a coastal Antarctic site and DOM molecularly characterised using ultrahigh-resolution mass spectrometry. We show that the biogeochemistry of DOM is highly complex and intimately connected with microbial and photochemical processes operating individually or in combination. Photo-biochemical processes resulted in shifts in the nitrogen, sulfur, and phosphorous content of the DOM. These processes are also an important mechanism for transforming refractory DOM, like dissolved black carbon and carboxylic rich alicyclic molecules from the snow surface. This study is unique, as it provides new molecular-level information on compounds that comprise the photo- and bio-labile, photo- and bio-refractory, as well as photo- and bio-produced fractions of the supraglacial DOM pool. These insights into the interactions between microbes, light, and specific components of the DOM pool highlight the need for studies focused on the biogeochemistry of supraglacial carbon and its response to a changing climate.

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References

  • Antony R, Grannas AM, Willoughby AS, Sleighter RL, Thamban M, Hatcher PG (2014) Origin and sources of dissolved organic matter in snow on the East Antarctic ice sheet. Environ Sci Technol 48:6151–6159

    Article  Google Scholar 

  • Antony R, Sanyal A, Kapse N, Dhakephalkar PK, Thamban M, Nair S (2016) Microbial communities associated with Antarctic snow pack and their biogeochemical implications. Microbiol Res 192:192–202

    Article  Google Scholar 

  • Antony R, Willoughby AS, Grannas AM, Catanzano V, Sleighter RL, Thamban M, Hatcher PG, Nair S (2017) Molecular insights on dissolved organic matter transformation by supraglacial microbial communities. Environ Sci Technol 51:4328–4337

    Article  Google Scholar 

  • Barker JD, Dubnick A, Lyons WB, Chin Y-P (2013) Changes in dissolved organic Matter (DOM) fluorescence in proglacial antarctic streams. Arct Antarct Alp Res 45(3):305–317

    Article  Google Scholar 

  • Benner R, Biddanda B (1998) Photochemical transformations of surface and deep marine dissolved organic matter: effects on bacterial growth. Limnol Oceanogr 43:1373–1378

    Article  Google Scholar 

  • Benner R, Ziegler S (1999) Do photochemical transformations of dissolved organic matter produce biorefractory as well as bioreactive substrates? In: Bell C, Brylinsky M, Johnson-Green PC (eds) Microbial Biosystems: New Frontiers. Proceedings of the 8th international symposium on microbial ecology. Atlantic Canada Society for Microbial Ecology, Canada, pp 181–192

  • Bhatia MP, Das SB, Longnecker K, Charette MA, Kujawinski EB (2010) Molecular characterization of dissolved organic matter associated with the Greenland ice sheet. Geochim Cosmochim Acta 74:3768–3784

    Article  Google Scholar 

  • Bushaw KL, Zepp RG, Tarr MA, Schulz-Jander D, Bourbonniere RA, Hodson RE, Miller WLD, Bronk A, Moran MA (1996) Photochemical release of biologically labile nitrogen from dissolved organic matter. Nature 381:404–407

    Article  Google Scholar 

  • Bushaw-Newton KL, Moran MA (1999) Photochemical formation of biologically available nitrogen from dissolved humic substances in coastal marine systems. Aquat Microb Ecol 18:285–292

    Article  Google Scholar 

  • Cook JM, Hodson AJ, Anesio AM, Hanna E, Yallop M, Stibal M, Telling J, Huybrechts P (2012) An improved estimate of microbially mediated carbon fluxes from the Greenland ice sheet. J Glaciol 58:1098–1108

    Article  Google Scholar 

  • Cory RM, Kling GW (2018) Interactions between sunlight and microorganisms influence dissolved organic matter degradation along the aquatic continuum. Limnol Oceanogr Lett 3:102–116

    Article  Google Scholar 

  • D’Andrilli J, Smith HJ, Dieser M, Foreman CM (2017) Climate driven carbon and microbial signatures through the last ice age. Geochem Perspect Let 4:29–34

    Article  Google Scholar 

  • D’Andrilli J, Cooper WT, Foreman CM, Marshall AG (2015) An ultrahigh-resolution mass spectrometry index to estimate natural organic matter lability. Rapid Commun Mass Spectrom 29:2385–2401

    Article  Google Scholar 

  • Dittmar T, Paeng J (2009) A heat-induced molecular signature in marine dissolved organic matter. Nat Geosci 2:175–179

    Article  Google Scholar 

  • Dittmar T, Koch B, Hertkorn N, Kattner G (2008) A simple and efficient method for the solid-phase extraction of dissolved organic matter (SPE-DOM) from seawater. Limnol Oceanogr 6:230–235

    Article  Google Scholar 

  • Fasching C, Behounek B, Singer GA, Battin TJ (2014) Microbial degradation of terrigenous dissolved organic matter and potential consequences for carbon cycling in brown-water streams. Sci Rep 4:4981

    Article  Google Scholar 

  • Franko DA, Heath RT (1982) UV-sensitive complex phosphorus: association with dissolved humic material and iron in a bog lake. Limnol Oceanogr 27:564–569

    Article  Google Scholar 

  • Gonsior M, Peake BM, Cooper WT, Podgorski D, D’Andrilli J, Cooper WJ (2009) Photochemically induced changes in dissolved organic matter identified by ultrahigh resolution fourier transform ion cyclotron resonance mass spectrometry. Environ Sci Technol 43:698–703

    Article  Google Scholar 

  • Gonsior M, Peake BM, Cooper WT, Podgorski DC, D’Andrilli J, Dittmar T, Cooper WJ (2011) Characterization of dissolved organic matter across the Subtropical Convergence off the South Island, New Zealand. Mar Chem 123:99–110

    Article  Google Scholar 

  • Goutx M, Acquaviva M, Bertrand J-C (1990) Cellular and extracellular carbohydrates and lipids from marine bacteria during growth on soluble substrates and hydrocarbons. Mar Ecol Prog Ser 61:291–296

    Article  Google Scholar 

  • Grannas AM, Shepson PB, Filley TR (2004) The photo-chemistry and nature of organic matter in Arctic and Antarctic Snow. Global Biogeochem Cycles 18:GB1006

    Article  Google Scholar 

  • Grannas AM, Hockaday WC, Hatcher PG, Thompson LG, Mosley-Thompson E (2006) New revelations on the nature of organic matter in ice cores. J Geophys Res 111:D04304

    Article  Google Scholar 

  • Grannas AM, Jones AE, Dibb J, Ammann M, Anastasio C, Beine HJ, Bergin M, Bottenheim J, Boxe CS, Carver G, Chen G, Crawford JH, Dominé F, Frey MM, Guzmán MI, Heard DE, Helmig D, Hoffmann MR, Honrath RE, Huey LG, Hutterli M, Jacobi HW, Klán P, Lefer B, McConnell J, Plane J, Sander R, Savarino J, Shepson PB, Simpson WR, Sodeau JR, von Glasow R, Weller R, Wolff EW, Zhu T (2007) An overview of snow photochemistry: evidence, mechanisms and impacts. Atmos Chem Phys 7:4329–4373

    Article  Google Scholar 

  • Hedges JI, Keil RG, Benner R (1997) What happens to terrestrial organic matter in the ocean? Org Geochem 27:195–212

    Article  Google Scholar 

  • Hertkorn N, Benner R, Frommberger M, Schmitt-Kopplin P, Witt M, Kaiser K, Kettrup A, Hedges JI (2006) Characterization of a major refractory component of marine dissolved organic matter. Geochim Cosmochim Acta 70(12):2990–3010

    Article  Google Scholar 

  • Herzsprung P, Hertkorn N, Friese K, Schmitt-Kopplin P (2010) Photochemical degradation of natural organic sulphur compounds (CHOS) from iron-rich mine pit lake pore waters—an initial understanding from evaluation of single elemental formulae using ultra-high-resolution mass spectrometry. Rapid Commun Mass Spectrom 24:2909–2924

    Article  Google Scholar 

  • Hockaday WC, Grannas AM, Kim S, Hatcher PG (2006) Direct molecular evidence for the degradation and mobility of black carbon in soils from the ultrahigh-resolution mass spectral analysis of dissolved organic matter from a fire-impacted forest soil. Org Geochem 37:501–510

    Article  Google Scholar 

  • Hockaday WC, Purcell JM, Marshall AG, Baldock JA, Hatcher PG (2009) Electrospray and photoionization mass spectrometry for the characterization of organic matter in natural waters: a qualitative assessment. Limnol Oceanogr Methods 7:81–95

    Article  Google Scholar 

  • Hood E, Fellman J, Spencer RGM, Hernes PJ, Edwards R, D’Amore D, Scott D (2009) Glaciers as a source of ancient and labile organic matter to the marine environment. Nature 462:1044–1048

    Article  Google Scholar 

  • Hood E, Battin TJ, Fellman J, O’Neel S, Spencer RGM (2015) Storage and release of organic carbon from glaciers and ice sheets. Nat Geosci 8:91–96

    Article  Google Scholar 

  • Kellerman AM, Dittmar T, Kothawala DN, Tranvik LJ (2014) Chemodiversity of dissolved organic matter in lakes driven by climate and hydrology. Nat Commun 5:3804

    Article  Google Scholar 

  • Kido Soule MC, Longnecker K, Giovannoni SJ, Kujawinski EB (2010) Impact of instrument and experimental parameters on the repeatability and reproducibility of peaks in ultrahigh resolution ESI FTICR mass spectra of natural organic matter. Org Geochem 41:725–733

    Article  Google Scholar 

  • Kieber DJ, McDaniel J, Mopper K (1989) Photochemical source of biological substrates in sea water—implications for carbon cycling. Nature 341:637–639

    Article  Google Scholar 

  • Kieber RJ, Li A, Seaton PJ (1999) Production of nitrite from the photodegradation of dissolved organic matter in natural waters. Environ Sci Technol 33:993–998

    Article  Google Scholar 

  • Koch BP, Dittmar T (2006) From mass to structure: an aromaticity index for high-resolution mass data of natural organic matter. Rapid Commun Mass Spectrom 20(5):926–932

    Article  Google Scholar 

  • Koch BP, Dittmar T (2016) Erratum of: From mass to structure: an aromaticity index for high-resolution mass data of natural organic matter. Rapid Commun Mass Spectrom 30:250

    Article  Google Scholar 

  • Koch BP, Witt M, Engbrodt R, Dittmar T, Kattner G (2005) Molecular formulae of marine and terrigenous dissolved organic matter detected by electrospray ionization Fourier transform ion cyclotron resonance mass spectrometry. Geochim Cosmochim Acta 69:3299–3308

    Article  Google Scholar 

  • Kragh T, Søndergaard M, Tranvik L (2008) Effect of exposure to sunlight and phosphorus limitation on bacterial degradation of coloured dissolved organic matter (CDOM) in freshwater. FEMS Microbiol Ecol 64:230–239

    Article  Google Scholar 

  • Kujawinski EB, Behn MD (2006) Automated analysis of electrospray ionization Fourier transform ion cyclotron resonance mass spectra of natural organic matter. Anal Chem 78:4363–4373

    Article  Google Scholar 

  • Laurion I, Mladenov N (2013) Dissolved organic matter photolysis in Canadian arctic thaw ponds. Environ Res Lett 8:035026

    Article  Google Scholar 

  • Lindell MJ, Graneèli W, Tranvik LJ (1995) Enhanced bacterial growth in response to photochemical transformation of dissolved organic matter. Limnol Oceanogr 40:195–199

    Article  Google Scholar 

  • Mazzoleni LR, Saranjampour P, Dalbec MM, Samburova V, Hallar AG, Zielinska B, Lowenthal D, Kohl S (2012) Identification of water-soluble organic carbon in nonurban aerosols using ultra-high resolution FT-ICR mass spectrometry: organic anions. Environ Chem 9:285–297

    Article  Google Scholar 

  • McCallister SL, del Giorgio PA (2012) Evidence for the respiration of ancient terrestrial organic C in northern temperate lakes and streams. Proc Natl Acad Sci USA 109:16963–16968

    Article  Google Scholar 

  • McNeill VF, Grannas AM, Abbatt JPD, Ammann M, Ariya P, Bartels-Rausch T, Domine F, Donaldson DJ, Guzman MI, Heger D, Kahan TF, Klán P, Masclin S, Toubin C, Voisin D (2012) Organics in environmental ices: sources, chemistry, and impacts. Atmos Chem Phys 12:9653–9678

    Article  Google Scholar 

  • Mopper K, Kieber DJ (2002) Photochemistry and the cycling of carbon, nitrogen and phosphorus. In: Hansell DA, Carlson CA (eds) Biogeochemistry of marine dissolved organic matter. Academic Press, USA, pp 456–507

    Google Scholar 

  • Moran MA, Zepp RG (1997) Role of photoreactions in the formation of biologically labile compounds from dissolved organic matter. Limnol Oceanogr 42:1307–1316

    Article  Google Scholar 

  • Moran MA, Zepp RG (2000) UV radiation effects on microbes and microbial processes. In: Kirchman DL (ed) Microbial ecology of the oceans. Wiley-Liss, New York, pp 201–228

    Google Scholar 

  • Musilova M, Tranter M, Wadham J, Telling J, Tedstone A, Anesio AM (2017) Microbially driven export of labile organic carbon from the Greenland ice sheet. Nat Geosci 10:360–365

    Article  Google Scholar 

  • Nelson DL, Cox MM (2000) Cells. In: Ryan M (ed) Principles of Biochemistry. Worth, New York, pp 21–50

    Google Scholar 

  • Obernosterer I, Benner R (2004) Competition between biological and photochemical processes in the mineralization of dissolved organic carbon. Limnol Oceanogr 49:117–124

    Article  Google Scholar 

  • Ohno T, He Z, Sleighter RL, Honeycutt C, Hatcher PG (2010) Ultrahigh resolution mass spectrometry and indicator species analysis to identify marker components of soil and plant biomass-derived organic matter fractions. Environ Sci Technol 44(22):8594–8600

    Article  Google Scholar 

  • Pautler BG, Simpson AJ, Simpson MJ, Tseng L-H, Spraul M, Dubnick A, Sharp MJ, Fitzsimmons SJ (2011) Detection and structural identification of dissolved organic matter in Antarctic glacial ice at natural abundance by SPR-W5-WATE RGATE 1H NMR spectroscopy. Environ Sci Technol 45:4710–4717

    Article  Google Scholar 

  • Priscu JC, Tulaczyk S, Studinger M, Kennicutt MC II, Christner BC, Foreman CM (2008) Antarctic subglacial water: origin, evolution, and ecology. In: Vincent WF, Laybourn-Parry J (eds) Polar lakes and rivers. Oxford University Press, UK, pp 119–136

    Chapter  Google Scholar 

  • Rignot E, Jacobs S, Mouginot J, Scheuchl B (2013) Ice-shelf melting around Antarctica. Science 341:266–270

    Article  Google Scholar 

  • Rossel PE, Vähätalo AV, Witt M, Dittmar T (2013) Molecular composition of dissolved organic matter from a wetland plant (Juncus effusus) after photochemical and microbial decomposition (125 year): common features with deep sea dissolved organic matter. Org Geochem 60:62–71

    Article  Google Scholar 

  • Schmidt F, Elvert M, Koch BP, Witt M, Kai-Uwe H (2009) Molecular characterization of dissolved organic matter in pore water of continental shelf sediments. Geochim Cosmochim Acta 73:3337–3358

    Article  Google Scholar 

  • Shepherd A, Ivins ER, Geruo A, IMBIE Project Group (2012) A reconciled estimate of ice-sheet mass balance. Science 338:1183–1189

    Article  Google Scholar 

  • Singer GA, Fasching C, Wilhelm L, Niggemann J, Steier P, Dittmar T, Battin TJ (2012) Biogeochemically diverse organic matter in Alpine glaciers and its downstream fate. Nat Geosci 5:710–714

    Article  Google Scholar 

  • Sleighter RL, Hatcher PG (2008) Molecular characterization of dissolved organic matter (DOM) along a river to ocean transect of the lower Chesapeake Bay by ultrahigh resolution electrospray ionization Fourier transform ion cyclotron resonance mass spectrometry. Mar Chem 110(3–4):140–152

    Article  Google Scholar 

  • Sleighter RL, McKee GA, Liu Z, Hatcher PG (2008) Naturally present fatty acids as internal calibrants for Fourier transform mass spectra of dissolved organic matter. Limnol Oceanogr Methods 6:246–253

    Article  Google Scholar 

  • Sleighter RL, Liu Z, Xue J, Hatcher PG (2010) Multivariate statistical approaches for the characterization of dissolved organic matter analyzed by ultrahigh resolution mass spectrometry. Environ Sci Technol 44(19):7576–7582

    Article  Google Scholar 

  • Sleighter RL, Chen H, Wozniak AS, Willoughby AS, Caricasole P, Hatcher PG (2012) Establishing a measure of reproducibility of ultrahigh-resolution mass spectra for complex mixtures of natural organic matter. Anal Chem 84:9184–9191

    Article  Google Scholar 

  • Smith HJ, Foster RA, McKnight DM, Lisle JT, Littmann S, Kuypers MMM, Foreman CM (2017) Microbial formation of labile organic carbon in Antarctic glacial environments. Nat Geosci 10:356–359

    Article  Google Scholar 

  • Stibal M, Šabacká M, Žárský J (2012) Biological processes on glacier and ice sheet surfaces. Nat Geosci 5:771–774

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Stubbins A, Hood E, Raymond PA, Aiken GR, Sleighter RL, Hernes PJ, Butman D, Hatcher PG, Striegl RG, Schuster P, Abdulla HAN, Vermilyea AW, Scott DT, Spencer RGM (2012) Anthropogenic aerosols as a source of ancient dissolved organic matter in glaciers. Nat Geosci 5:198–201

    Article  Google Scholar 

  • Thornton DCO (2014) Dissolved organic matter (DOM) release by phytoplankton in the contemporary and future ocean. Eur J Phycol 49:20–46

    Article  Google Scholar 

  • Tranvik LJ, Kokalj S (1998) Decreased biodegradability of algal DOC due to interactive effects of UV radiation and humic matter. Aquat Microb Ecol 14:301–307

    Article  Google Scholar 

  • Tranvik LJ, Olofsson H, Bertilsson S (2000) Photochemical effects on bacterial degradation of dissolved organic matter in lake water. In: Bell CR, Brylinsky M, Johnson-Green P (eds) Microbial biosystems: new frontiers proceedings of the 8th international symposium on microbial ecology, Atlantic Canada Society for Microbial Ecology, Canada, pp 193–200

  • Vähätalo AV, Järvinen M (2007) Photochemically produced bioavailable nitrogen from biologically recalcitrant dissolved organic matter stimulates production of a nitrogen-limited microbial food web in the Baltic Sea. Limnol Oceanogr 52:132–143

    Article  Google Scholar 

  • Vähätalo AV, Salonen K, Münster U, Järvinen M, Wetzel RG (2003) Photochemical transformation of allochthonous organic matter provides bioavailable nutrients in a humic lake. Arch Hydrobiol 156:287–314

    Article  Google Scholar 

  • Vähätalo AV, Aarnos H, Hoikkala L, Lignell R (2011) Photochemical transformation of terrestrial dissolved organic matter supports hetero- and autotrophic production in coastal waters. Mar Ecol Prog Ser 423:1–14

    Article  Google Scholar 

  • Ward ND, Keil RG, Medeiros PM, Brito DC, Cunha AC, Dittmar T, Yager PL, Krusche AV, Richey JE (2013) Degradation of terrestrially derived macromolecules in the Amazon River. Nat Geosci 6:530–533

    Article  Google Scholar 

  • Wetzel RG, Hatcher PG, Bianchi TS (1995) Natural photolysis by ultraviolet irradiance of recalcitrant dissolved organic matter to simple substrates for rapid bacterial metabolism. Limnol Oceanogr 40:1369–1380

    Article  Google Scholar 

  • Xu JZ, Grannas A, Xiao CD, Du ZH, Willoughby A, Hatcher P, An YQ (2018) High-resolution mass spectrometric characterization of dissolved organic matter from warm and cold periods in the NEEM ice core. Sci Cold Arid Reg 10:38–46

    Google Scholar 

  • Yavitt JB, Fahey TJ (1984) An experimental analysis of solution chemistry in a lodgepole pine forest floor. Oikos 43:222–234

    Article  Google Scholar 

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Acknowledgements

We thank the Ministry of Earth Sciences (India) and the Director, NCAOR for support. We are grateful for the support from the members and crew of the 33rd Indian Scientific Expedition to Antarctica. Shri M. J. Beg, Director (Logistics), NCAOR, is thanked for providing all necessary logistic support for the sampling, as well as, for the safe transport of samples to Old Dominion University. We also thank the College of Sciences Major Instrumentation Cluster at ODU for their assistance with the FTICR-MS data acquisition. The FTICR-MS analysis was funded by the National Science Foundation (Antarctic Glaciology Program #0739691). We also appreciate the constructive comments provided by reviewers, which allowed us to greatly improve the quality of this manuscript. This is NCAOR contribution number 55/2018.

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Authors and Affiliations

  1. National Centre for Antarctic and Ocean Research, Headland Sada, Vasco-Da-Gama, Goa, 403 804, India

    Runa Antony & Meloth Thamban

  2. Department of Chemistry and Biochemistry, Old Dominion University, Norfolk, VA, 23529, USA

    Amanda S. Willoughby, Rachel L. Sleighter & Patrick G. Hatcher

  3. Department of Chemistry, Villanova University, Villanova, PA, 19085, USA

    Amanda M. Grannas & Victoria Catanzano

  4. FBSciences, Inc. (Research and Development), Norfolk, VA, 23508, USA

    Rachel L. Sleighter

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  1. Runa Antony
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Correspondence to Runa Antony.

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Antony, R., Willoughby, A.S., Grannas, A.M. et al. Photo-biochemical transformation of dissolved organic matter on the surface of the coastal East Antarctic ice sheet. Biogeochemistry 141, 229–247 (2018). https://doi.org/10.1007/s10533-018-0516-0

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