Potential utilization of terrestrially derived dissolved organic matter by aquatic microbial communities in saline lakes

Abstract

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, ActinobacteriaBacteroidia, BacilliGammaproteobacteriaHalobacteria, PlanctomycetaciaRhodothermia, 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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Fig. 1
Fig. 2: Difference of DOM molecular composition in the studied lake microcosms.
Fig. 3: Networks showing the associations between microbial operational taxonomic units (OTUs) and DOM molecular formulae in the experimental treatments.
Fig. 4

References

  1. 1.

    Wetzel RG. Limnology: lake and river ecosystems, 3rd ed. San Diego, CA: Academic Press; 2001. p. 15–40.

  2. 2.

    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.

    CAS  Google Scholar 

  3. 3.

    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.

    Google Scholar 

  4. 4.

    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.

    Google Scholar 

  5. 5.

    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.

    PubMed  Google Scholar 

  6. 6.

    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.

    CAS  Google Scholar 

  7. 7.

    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.

    Google Scholar 

  8. 8.

    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.

    CAS  PubMed  Google Scholar 

  9. 9.

    Nebbioso A, Piccolo A. Molecular characterization of dissolved organic matter (DOM): a critical review. Anal Bioanal Chem. 2013;405:109–24.

    CAS  PubMed  Google Scholar 

  10. 10.

    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.

    PubMed  Google Scholar 

  11. 11.

    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.

    PubMed  PubMed Central  Google Scholar 

  12. 12.

    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.

    CAS  PubMed  Google Scholar 

  13. 13.

    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.

    CAS  Google Scholar 

  14. 14.

    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.

    CAS  PubMed  Google Scholar 

  15. 15.

    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.

    CAS  PubMed  Google Scholar 

  16. 16.

    Zheng M. An introduction to saline lakes on the Qinghai-Tibet plateau, 1st ed. Dordrecht: Kluwer Academic Publisher; 1997. p. 1–17.

  17. 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.

    CAS  PubMed  Google Scholar 

  18. 18.

    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.

    CAS  Google Scholar 

  19. 19.

    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.

    CAS  PubMed  Google Scholar 

  20. 20.

    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.

    CAS  Google Scholar 

  21. 21.

    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.

    CAS  Google Scholar 

  22. 22.

    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.

    CAS  PubMed  PubMed Central  Google Scholar 

  23. 23.

    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.

    CAS  PubMed  PubMed Central  Google Scholar 

  24. 24.

    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.

    CAS  PubMed  PubMed Central  Google Scholar 

  25. 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  26. 26.

    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.

    CAS  Google Scholar 

  27. 27.

    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.

    CAS  PubMed  PubMed Central  Google Scholar 

  28. 28.

    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.

    CAS  PubMed  PubMed Central  Google Scholar 

  29. 29.

    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.

    Google Scholar 

  30. 30.

    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.

    CAS  Google Scholar 

  31. 31.

    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.

    CAS  PubMed  PubMed Central  Google Scholar 

  32. 32.

    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.

    CAS  Google Scholar 

  33. 33.

    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.

    PubMed  PubMed Central  Google Scholar 

  34. 34.

    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.

    CAS  PubMed  PubMed Central  Google Scholar 

  35. 35.

    Krevelen DW. Graphical-statistical method for the study of structure and reaction processes of coal. Fuel. 1961;29:269–83.

    Google Scholar 

  36. 36.

    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.

    Google Scholar 

  37. 37.

    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.

  38. 38.

    Clauset A, Newman MEJ, Moore C. Finding community structure in very large networks. Phys Rev E. 2004;70:066111.

    Google Scholar 

  39. 39.

    Guimerà R, Nunes Amaral LA. Functional cartography of complex metabolic networks. Nature. 2005;433:895–900.

    PubMed  PubMed Central  Google Scholar 

  40. 40.

    Deng Y, Jiang Y-H, Yang Y, He Z, Luo F, Zhou J. Molecular ecological network analyses. BMC Bioinforma. 2012;13:113.

    Google Scholar 

  41. 41.

    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.

    PubMed  PubMed Central  Google Scholar 

  42. 42.

    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.

    CAS  PubMed  Google Scholar 

  43. 43.

    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.

    CAS  PubMed  Google Scholar 

  44. 44.

    Newman MEJ. Modularity and community structure in networks. Proc Natl Acad Sci USA. 2006;103:8577–82.

    CAS  PubMed  Google Scholar 

  45. 45.

    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.

    CAS  Google Scholar 

  46. 46.

    Raymond PA, Bauer JE. Bacterial consumption of DOC during transport through a temperate estuary. Aquat Micro Ecol. 2000;22:1–12.

    Google Scholar 

  47. 47.

    del Giorgio PA, Duarte CM. Respiration in the open ocean. Nature. 2002;420:379–84.

    PubMed  Google Scholar 

  48. 48.

    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.

    CAS  PubMed  Google Scholar 

  49. 49.

    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.

    CAS  Google Scholar 

  50. 50.

    Bugg TDH, Ahmad M, Hardiman EM, Rahmanpour R. Pathways for degradation of lignin in bacteria and fungi. Nat Prod Rep. 2011a;28:1883–96.

    CAS  PubMed  Google Scholar 

  51. 51.

    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.

    CAS  PubMed  Google Scholar 

  52. 52.

    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.

    Google Scholar 

  53. 53.

    Pollegioni L, Tonin F, Rosini E. Lignin-degrading enzymes. FEBS J. 2015;282:1190–213.

    CAS  PubMed  Google Scholar 

  54. 54.

    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.

    PubMed  Google Scholar 

  55. 55.

    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.

    CAS  PubMed  Google Scholar 

  56. 56.

    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.

    CAS  PubMed  Google Scholar 

  57. 57.

    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.

    CAS  PubMed  Google Scholar 

  58. 58.

    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.

    CAS  PubMed  Google Scholar 

  59. 59.

    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.

    CAS  Google Scholar 

  60. 60.

    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.

    CAS  Google Scholar 

  61. 61.

    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.

    PubMed  PubMed Central  Google Scholar 

  62. 62.

    Zimmerman AE, Martiny AC, Allison SD. Microdiversity of extracellular enzyme genes among sequenced prokaryotic genomes. ISME J. 2013;7:1187.

    CAS  PubMed  PubMed Central  Google Scholar 

  63. 63.

    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.

    CAS  PubMed  PubMed Central  Google Scholar 

  64. 64.

    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.

    PubMed  Google Scholar 

  65. 65.

    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.

    Google Scholar 

  66. 66.

    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.

    CAS  PubMed  Google Scholar 

  67. 67.

    Zhou J, Deng Y, Luo F, He Z, Tu Q, Zhi X. Functional molecular ecological networks. MBio. 2010;1:e00169–00110.

    PubMed  PubMed Central  Google Scholar 

  68. 68.

    Zark M, Dittmar T. Universal molecular structures in natural dissolved organic matter. Nat Commun. 2018;9:3178.

    PubMed  PubMed Central  Google Scholar 

  69. 69.

    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.

    CAS  PubMed  Google Scholar 

  70. 70.

    Oren A. Thermodynamic limits to microbial life at high salt concentrations. Environ Microbiol. 2011;13:1908–23.

    CAS  PubMed  Google Scholar 

  71. 71.

    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.

    CAS  PubMed  PubMed Central  Google Scholar 

  72. 72.

    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.

    PubMed  PubMed Central  Google Scholar 

  73. 73.

    Godwin CM, Cotner JB. Aquatic heterotrophic bacteria have highly flexible phosphorus content and biomass stoichiometry. ISME J. 2015;9:2324.

    CAS  PubMed  PubMed Central  Google Scholar 

  74. 74.

    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.

    Google Scholar 

  75. 75.

    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.

    Google Scholar 

  76. 76.

    Spohn M. Element cycling as driven by stoichiometric homeostasis of soil microorganisms. Basic Appl Ecol. 2016;17:471–8.

    Google Scholar 

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Acknowledgements

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

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