Lakes receive large amounts of terrestrially derived dissolved organic matter (tDOM). However, little is known about how aquatic microbial communities interact with tDOM in lakes. Here, by performing microcosm experiments we investigated how microbial community responded to tDOM influx in six Tibetan lakes of different salinities (ranging from 1 to 358 g/l). In response to tDOM addition, microbial biomass increased while dissolved organic carbon (DOC) decreased. The amount of DOC decrease did not show any significant correlation with salinity. However, salinity influenced tDOM transformation, i.e., microbial communities from higher salinity lakes exhibited a stronger ability to utilize tDOM of high carbon numbers than those from lower salinity. Abundant taxa and copiotrophs were actively involved in tDOM transformation, suggesting their vital roles in lacustrine carbon cycle. Network analysis indicated that 66 operational taxonomic units (OTUs, affiliated with Alphaproteobacteria, Actinobacteria, Bacteroidia, Bacilli, Gammaproteobacteria, Halobacteria, Planctomycetacia, Rhodothermia, and Verrucomicrobiae) were associated with degradation of CHO compounds, while four bacterial OTUs (affiliated with Actinobacteria, Alphaproteobacteria, Bacteroidia and Gammaproteobacteria) were highly associated with the degradation of CHOS compounds. Network analysis further revealed that tDOM transformation may be a synergestic process, involving cooperation among multiple species. In summary, our study provides new insights into a microbial role in transforming tDOM in saline lakes and has important implications for understanding the carbon cycle in aquatic environments.
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Wetzel RG. Limnology: lake and river ecosystems, 3rd ed. San Diego, CA: Academic Press; 2001. p. 15–40.
Song K, Wen Z, Shang Y, Yang H, Lyu L, Liu G, et al. Quantification of dissolved organic carbon (DOC) storage in lakes and reservoirs of mainland China. J Environ Manag. 2018;217:391–402.
Wen Z, Song K, Shang Y, Zhao Y, Fang C, Lyu L. Differences in the distribution and optical properties of DOM between fresh and saline lakes in a semi-arid area of Northern China. Aquat Sci. 2018;80:22.
Duarte CM, Prairie YT, Montes C, Cole JJ, Striegl R, Melack J, et al. CO2 emissions from saline lakes: a global estimate of a surprisingly large flux. J Geophys Res: Biogeosci. 2008;113:G04041.
Jansson M, Persson L, De Roos AM, Jones RI, Tranvik LJ. Terrestrial carbon and intraspecific size-variation shape lake ecosystems. Trends Ecol Evol. 2007;22:316–22.
Tranvik LJ, Downing JA, Cotner JB, Loiselle SA, Striegl RG, Ballatore TJ, et al. Lakes and reservoirs as regulators of carbon cycling and climate. Limnol Oceanogr. 2009;54:2298–314.
Cole JJ, Prairie YT, Caraco NF, McDowell WH, Tranvik LJ, Striegl RG, et al. Plumbing the global carbon cycle: integrating inland waters into the terrestrial carbon budget. Ecosystems. 2007;10:172–85.
Kellerman AM, Dittmar T, Kothawala DN, Tranvik LJ. Chemodiversity of dissolved organic matter in lakes driven by climate and hydrology. Nat Commun. 2014;5:3804.
Nebbioso A, Piccolo A. Molecular characterization of dissolved organic matter (DOM): a critical review. Anal Bioanal Chem. 2013;405:109–24.
Lapierre J-F, Guillemette F, Berggren M, del Giorgio PA. Increases in terrestrially derived carbon stimulate organic carbon processing and CO2 emissions in boreal aquatic ecosystems. Nat Commun. 2013;4:2972.
Logue JB, Stedmon CA, Kellerman AM, Nielsen NJ, Andersson AF, Laudon H, et al. Experimental insights into the importance of aquatic bacterial community composition to the degradation of dissolved organic matter. ISME J. 2015;10:533.
McCallister SL, del Giorgio PA. Evidence for the respiration of ancient terrestrial organic C in northern temperate lakes and streams. Proc Natl Acad Sci USA. 2012;109:16963–8.
Ward ND, Keil RG, Medeiros PM, Brito DC, Cunha AC, Dittmar T, et al. Degradation of terrestrially derived macromolecules in the Amazon River. Nat Geosci. 2013;6:530–3.
Gudasz C, Bastviken D, Steger K, Premke K, Sobek S, Tranvik LJ. Temperature-controlled organic carbon mineralization in lake sediments. Nature. 2010;466:478–81.
Jiao N, Herndl GJ, Hansell DA, Benner R, Kattner G, Wilhelm SW, et al. Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nat Rev Microbiol. 2010;8:593–9.
Zheng M. An introduction to saline lakes on the Qinghai-Tibet plateau, 1st ed. Dordrecht: Kluwer Academic Publisher; 1997. p. 1–17.
Song K, Shang Y, Wen Z, Jacinthe P-A, Liu G, Lyu L, et al. Characterization of CDOM in saline and freshwater lakes across China using spectroscopic analysis. Water Res. 2019;150:403–17.
Spencer RGM, Guo W, Raymond PA, Dittmar T, Hood E, Fellman J, et al. Source and biolability of ancient dissolved organic matter in glacier and lake ecosystems on the Tibetan Plateau. Geochim Cosmochim Acta. 2014;142:64–74.
Jiang H, Dong H, Yu B, Liu X, Li Y, Ji S, et al. Microbial response to salinity change in Lake Chaka, a hypersaline lake on Tibetan plateau. Environ Microbiol. 2007;9:2603–21.
Jiang H, Dong CZ, Huang Q, Wang G, Fang B, Zhang C, et al. Actinobacterial diversity in microbial mats of five hot springs in central and central-eastern Tibet, China. Geomicrobiol J. 2012;29:520–7.
Liu Y, Yao T, Jiao N, Zhu L, Hu A, Liu X, et al. Salinity impact on bacterial community composition in five high-altitude lakes from the Tibetan plateau, Western China. Geomicrobiol J. 2013;30:462–9.
Wang J, Yang D, Zhang Y, Shen J, Van Der Gast C, Hahn MW, et al. Do patterns of bacterial diversity along salinity gradients differ from those observed for macroorganisms? PLoS ONE. 2011;6:e27597.
Wu QL, Zwart G, Schauer M, Kamst-van Agterveld MP, Hahn MW. Bacterioplankton community composition along a salinity gradient of sixteen high-mountain lakes located on the Tibetan Plateau, China. Appl Environ Microbiol. 2006;72:5478–85.
Xing P, Hahn MW, Wu QL. Low taxon richness of bacterioplankton in high-altitude lakes of the eastern Tibetan Plateau, with a predominance of Bacteroidetes and Synechococcus spp. Appl Environ Microbiol. 2009;75:7017–25.
Yang J, Ma LA, Jiang H, Wu G, Dong H. Salinity shapes microbial diversity and community structure in surface sediments of the Qinghai-Tibetan Lakes. Sci Rep. 2016;6:25078.
Yang J, Jiang H, Wu G, Liu W. Phylum-level archaeal distributions in the sediments of Chinese lakes with a large range of salinity. Geomicrobiol J. 2018;35:404–10.
Zhong Z-P, Liu Y, Miao L-L, Wang F, Chu L-M, Wang J-L, et al. Prokaryotic community structure driven by salinity and ionic concentrations in plateau lakes of the Tibetan Plateau. Appl Environ Microbiol. 2016;82:1846–58.
Yang J, Jiang H, Dong H, Wang H, Wu G, Hou W, et al. amoA-encoding archaea and thaumarchaeol in the lakes on the northeastern Qinghai-Tibetan Plateau, China. Front Microbiol. 2013;4:329.
Neal C, Neal M, Wickham H. Phosphate measurement in natural waters: two examples of analytical problems associated with silica interference using phosphomolybdic acid methodologies. Sci Total Environ. 2000;251–2:511–22.
Willis RB, Montgomery ME, Allen PR. Improved method for manual, colorimetric determination of total Kjeldahl nitrogen using salicylate. J Agric Food Chem. 1996;44:1804–7.
Jiang H, Dong H, Zhang G, Yu B, Chapman LR, Fields MW. Microbial diversity in water and sediment of Lake Chaka, an athalassohaline lake in northwestern China. Appl Environ Microbiol. 2006;72:3832–45.
Dittmar T, Koch B, Hertkorn N, Kattner G. A simple and efficient method for the solid-phase extraction of dissolved organic matter (SPE-DOM) from seawater. Limnol Oceanogr Meth. 2008;6:230–5.
Walters W, Hyde ER, Berg-Lyons D, Ackermann G, Humphrey G, Parada A, et al. Improved bacterial 16S rRNA gene (V4 and V4-5) and fungal internal transcribed spacer marker gene primers for microbial community surveys. mSystems. 2015;1:e00009–00015.
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 2012;6:1621–4.
Krevelen DW. Graphical-statistical method for the study of structure and reaction processes of coal. Fuel. 1961;29:269–83.
Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B (Methodol). 1995;57:289–300.
Steinhauser D, Krall L, Müssig C, Büssis D, Usadel B. Correlation networks. In: Junker BH, Schreiber F, editors. Analysis of biological networks. Hoboken, New Jersey, USA: John Wiley & Sons; 2008. p. 305–33.
Clauset A, Newman MEJ, Moore C. Finding community structure in very large networks. Phys Rev E. 2004;70:066111.
Guimerà R, Nunes Amaral LA. Functional cartography of complex metabolic networks. Nature. 2005;433:895–900.
Deng Y, Jiang Y-H, Yang Y, He Z, Luo F, Zhou J. Molecular ecological network analyses. BMC Bioinforma. 2012;13:113.
Zhou J, Deng Y, Luo F, He Z, Yang Y. Phylogenetic molecular ecological network of soil microbial communities in response to elevated CO2. MBio. 2011;2:e00122–00111.
Nelson CE, Carlson CA. Tracking differential incorporation of dissolved organic carbon types among diverse lineages of Sargasso Sea bacterioplankton. Environ Microbiol. 2012;14:1500–16.
Painter SC, Lapworth DJ, Woodward EMS, Kroeger S, Evans CD, Mayor DJ, et al. Terrestrial dissolved organic matter distribution in the North Sea. Sci Total Environ. 2018;630:630–47.
Newman MEJ. Modularity and community structure in networks. Proc Natl Acad Sci USA. 2006;103:8577–82.
Boyer J, Dailey S, Gibson P, Rogers M, Mir-Gonzalez D. The role of dissolved organic matter bioavailability in promoting phytoplankton blooms in Florida Bay. Hydrobiologia. 2006;569:71–85.
Raymond PA, Bauer JE. Bacterial consumption of DOC during transport through a temperate estuary. Aquat Micro Ecol. 2000;22:1–12.
del Giorgio PA, Duarte CM. Respiration in the open ocean. Nature. 2002;420:379–84.
Sharma AK, Becker JW, Ottesen EA, Bryant JA, Duhamel S, Karl DM, et al. Distinct dissolved organic matter sources induce rapid transcriptional responses in coexisting populations of Prochlorococcus, Pelagibacter and the OM60 clade. Environ Microbiol. 2014;16:2815–30.
Magnabosco C, Lin LH, Dong H, Bomberg M, Ghiorse W, Stan-Lotter H, et al. The biomass and biodiversity of the continental subsurface. Nat Geosci. 2018;11:707–17.
Bugg TDH, Ahmad M, Hardiman EM, Rahmanpour R. Pathways for degradation of lignin in bacteria and fungi. Nat Prod Rep. 2011a;28:1883–96.
Bugg TDH, Ahmad M, Hardiman EM, Singh R. The emerging role for bacteria in lignin degradation and bio-product formation. Curr Opin Biotechnol. 2011b;22:394–400.
Medeiros PM, Seidel M, Gifford SM, Ballantyne F, Dittmar T, Whitman WB, et al. Microbially-mediated transformations of estuarine dissolved organic matter. Front Mar Sci. 2017;4:69.
Pollegioni L, Tonin F, Rosini E. Lignin-degrading enzymes. FEBS J. 2015;282:1190–213.
Hambright KD, Beyer JE, Easton JD, Zamor RM, Easton AC, Hallidayschult TC. The niche of an invasive marine microbe in a subtropical freshwater impoundment. ISME J. 2015;9:256–64.
Foti MJ, Sorokin DY, Zacharova EE, Pimenov NV, Kuenen JG, Muyzer G. Bacterial diversity and activity along a salinity gradient in soda lakes of the Kulunda Steppe (Altai, Russia). Extremophiles. 2008;12:133–45.
Logares R, Lindstrom ES, Langenheder S, Logue JB, Paterson H, Laybourn-Parry J, et al. Biogeography of bacterial communities exposed to progressive long-term environmental change. ISME J. 2013;7:937–48.
Hunt DE, David LA, Gevers D, Preheim SP, Alm EJ, Polz MF. Resource partitioning and sympatric differentiation among closely related bacterioplankton. Science. 2008;320:1081–5.
McCarren J, Becker JW, Repeta DJ, Shi Y, Young CR, Malmstrom RR, et al. Microbial community transcriptomes reveal microbes and metabolic pathways associated with dissolved organic matter turnover in the sea. Proc Natl Acad Sci USA. 2010;107:16420–7.
Mills MM, Moore CM, Langlois R, Milne A, Achterberg E, Nachtigall K, et al. Nitrogen and phosphorus co-limitation of bacterial productivity and growth in the oligotrophic subtropical North Atlantic. Limnol Oceanogr. 2008;53:824–34.
Carlson CA, Giovannoni SJ, Hansell DA, Goldberg SJ, Parsons R, Vergin K. Interactions among dissolved organic carbon, microbial processes, and community structure in the mesopelagic zone of the northwestern Sargasso Sea. Limnol Oceanogr. 2004;49:1073–83.
Herlemann DPR, Manecki M, Meeske C, Pollehne F, Labrenz M, Schulz-Bull D, et al. Uncoupling of bacterial and terrigenous dissolved organic matter dynamics in decomposition experiments. PLoS ONE. 2014;9:e93945.
Zimmerman AE, Martiny AC, Allison SD. Microdiversity of extracellular enzyme genes among sequenced prokaryotic genomes. ISME J. 2013;7:1187.
Cottrell MT, Kirchman DL. Natural assemblages of marine Proteobacteria and members of the Cytophaga-Flavobacter cluster consuming low- and high-molecular-weight dissolved organic matter. Appl Environ Microbiol. 2000;66:1692–7.
Gómez-Consarnau L, Lindh MV, Gasol JM, Pinhassi J. Structuring of bacterioplankton communities by specific dissolved organic carbon compounds. Environ Microbiol. 2012;14:2361–78.
Luo F, Zhong J, Yang Y, Zhou J. Application of random matrix theory to microarray data for discovering functional gene modules. Phys Rev E. 2006;73:031924.
Horemans B, Vandermaesen J, Smolders E, Springael D. Cooperative dissolved organic carbon assimilation by a linuron-degrading bacterial consortium. FEMS Microbiol Ecol. 2013;84:35–46.
Zhou J, Deng Y, Luo F, He Z, Tu Q, Zhi X. Functional molecular ecological networks. MBio. 2010;1:e00169–00110.
Zark M, Dittmar T. Universal molecular structures in natural dissolved organic matter. Nat Commun. 2018;9:3178.
Osterholz H, Niggemann J, Giebel H-A, Simon M, Dittmar T. Inefficient microbial production of refractory dissolved organic matter in the ocean. Nat Commun. 2015;6:7422.
Oren A. Thermodynamic limits to microbial life at high salt concentrations. Environ Microbiol. 2011;13:1908–23.
Cortes-Tolalpa L, Norder J, van Elsas JD, Falcao Salles J. Halotolerant microbial consortia able to degrade highly recalcitrant plant biomass substrate. Appl Microbiol Biotechnol. 2018;102:2913–27.
Sorokin DY, Toshchakov SV, Kolganova T, Kublanov IV. Halo(natrono)archaea isolated from hypersaline lakes utilize cellulose and chitin as growth substrates. Front Microbiol. 2015;6:942.
Godwin CM, Cotner JB. Aquatic heterotrophic bacteria have highly flexible phosphorus content and biomass stoichiometry. ISME J. 2015;9:2324.
Elser JJ, Sterner RW, Gorokhova E, Fagan WF, Markow TA, Cotner JB, et al. Biological stoichiometry from genes to ecosystems. Ecol Lett. 2000;3:540–50.
Manzoni S, Trofymow JA, Jackson RB, Porporato A. Stoichiometric controls on carbon, nitrogen, and phosphorus dynamics in decomposing litter. Ecol Monogr. 2010;80:89–106.
Spohn M. Element cycling as driven by stoichiometric homeostasis of soil microorganisms. Basic Appl Ecol. 2016;17:471–8.
This research was supported by grants from the National Natural Science Foundation of China (Grant Nos. 91751206, 41521001, 41972317, 41572328, and 41630103), the 111 Program (State Administration of Foreign Experts Affairs & the Ministry of Education of China, grant B18049), and Fundamental Research Funds for the Central Universities, China University of Geosciences (Wuhan), and State Key Laboratory of Biogeology and Environmental Geology, CUG (No. GBL11805). Portions of this work was performed in the W. R. Wiley Environmental Molecular Sciences Laboratory (EMSL), a DOE Office of Science User Facility sponsored by the Office of Biological and Environmental Research. We are grateful to anonymous reviewers for their constructive comments, which significantly improved the quality of the manuscript.
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Yang, J., Jiang, H., Liu, W. et al. Potential utilization of terrestrially derived dissolved organic matter by aquatic microbial communities in saline lakes. ISME J 14, 2313–2324 (2020). https://doi.org/10.1038/s41396-020-0689-0
Environmental Pollution (2021)