Temporal and Spatial Variations of Microbial Carbon Utilization in Water Bodies from the Dajiuhu Peatland, Central China

Abstract

To investigate the microbial utilization of organic carbon in peatland ecosystem, water samples were collected from the Dajiuhu Peatland and nearby lakes, central China across the year of 2014. The acridine orange (AO) staining and Biolog Eco microplates were used to numerate microbial counts and determine the carbon utilization of microbial communities. Meanwhile, physicochemical characteristics were measured for subsequent analysis of the correlation between microbial carbon utilization and environmental factors. Results indicated that total microbial counts were between 10⁶–10⁷ cells/L. Microbial diversities and carbon utilization rates showed a similar pattern, highest in September and lowest in November. Microbial communities in the peat pore waters preferred to utilize N-bearing carbon sources such as amines and amino acids compared with microbial communities in lakes. The network analysis of microbial utilization of 31 carbon substrates clearly distinguished microbial communities from peat pore waters and those from lakes. Redundancy analysis (RDA) showed the total organic nitrogen content (P=0.03, F=2.5) and daily average temperature (P=0.034, F=2.4) significantly controlled microbial carbon utilization throughout the sampling period. Our report is the first one to address the temporal and spatial variations of carbon utilization of microbial communities which are closely related to the decomposition of organic matter in the Dajiuhu Peatland in context of climate warming.

Keywords

carbon source / microbial carbon utilization / average temperature / Dajiuhu Peatland

References

[1] Archer D., Martin P., Buffett B., . The Importance of Ocean Temperature to Global Biogeochemistry. Earth and Planetary Science Letters, 2004, 222(2): 333-348.

[2] Armstrong A., Waldron S., Ostle N. J., . Biotic and Abiotic Factors Interact to Regulate Northern Peatland Carbon Cycling. Ecosystems, 2015, 18(8): 1395-1409.

[3] Barberán A., Bates S. T., Casamayor E. O., . Using Network Analysis to Explore Co–Occurrence Patterns in Soil Microbial Communities. The ISME Journal, 2012, 6(2): 343-351.

[4] Bastian M., Heymann S., Jacomy M. Gephi: An Open Source Software for Exploring and Manipulating Networks. ICWSM, 2009, 8: 361-362.

[5] Bending G. D., Putland C., Rayns F. Changes in Microbial Community Metabolism and Labile Organic Matter Fractions as Early Indicators of the Impact of Management on Soil Biological Quality. Biology and Fertility of Soils, 2000, 31(1): 78-84.

[6] Bengtsson F., Granath G., Rydin H. Photosynthesis, Growth, and Decay Traits in Sphagnum—A Multispecies Comparison. Ecology and Evolution, 2016, 6(10): 3325-3341.

[7] Berman T., Bronk D. Dissolved Organic Nitrogen: A Dynamic Participant in Aquatic Ecosystems. Aquatic Microbial Ecology, 2003, 31(3): 279-305.

[8] Bon C. E., Reeve A. S., Slater L., . Using Hydrologic Measurements to Investigate Free–Phase Gas Ebullition in a Maine Peatland, USA. Hydrology and Earth System Sciences, 2014, 18(3): 953-965.

[9] Bragina A., Berg C., Müller H., . Insights into Functional Bacterial Diversity and Its Effects on Alpine Bog Ecosystem Functioning. Scientific Reports, 2013, 3 6 1955

[10] Brown M. G., Humphreys E. R., Moore T. R., . Evidence for a Nonmonotonic Relationship between Ecosystem–Scale Peatland Methane Emissions and Water Table Depth. Journal of Geophysical Research: Biogeosciences, 2014, 119(5): 826-835.

[11] Brzostek E. R., Finzi A. C. Substrate Supply, Fine Roots, and Temperature Control Proteolytic Enzyme Activity in Temperate Forest Soils. Ecology, 2011, 92(4): 892-902.

[12] Bushaw–Newton K. L., Ewers E. C., Velinsky D. J., . Bacterial Community Profiles from Sediments of the Anacostia River Using Metabolic and Molecular Analyses. Environmental Science and Pollution Research, 2012, 19(4): 1271-1279.

[13] Busse M. D., Ratcliff A. W., Shestak C. J., . Glyphosate Toxicity and the Effects of Long–Term Vegetation Control on Soil Microbial Communities. Soil Biology and Biochemistry, 2001, 33(12/13): 1777-1789.

[14] Conan P., Joux F., Torréton J., . Effect of Solar Ultraviolet Radiation on Bacterio–and Phytoplankton Activity in a Large Coral Reef Lagoon (Southwest New Caledonia). Aquatic Microbial Ecology, 2008, 52: 83-98.

[15] Dahllöf I., Agrenius S., Blanck H., . The Effect of TBT on the Structure of a Marine Sediment Community—A Boxcosm Study. Marine Pollution Bulletin, 2001, 42(8): 689-695.

[16] Davidson E. A., Janssens I. A. Temperature Sensitivity of Soil Carbon Decomposition and Feedbacks to Climate Change. Nature, 2006, 440(7081): 165-173.

[17] Dijkstra P., Thomas S. C., Heinrich P. L., . Effect of Temperature on Metabolic Activity of Intact Microbial Communities: Evidence for Altered Metabolic Pathway Activity but not for Increased Maintenance Respiration and Reduced Carbon Use Efficiency. Soil Biology and Biochemistry, 2011, 43(10): 2023-2031.

[18] Foster R. A., Kuypers M. M. M., Vagner T., . Nitrogen Fixation and Transfer in Open Ocean Diatom–Cyanobacterial Symbioses. The ISME Journal, 2011, 5(9): 1484-1493.

[19] Francisco D. E., Mah R. A., Rabin A. C. Acridine Orange–Epifluorescence Technique for Counting Bacteria in Natural Waters. Transactions of the American Microscopical Society, 1973, 92(3): 416-421.

[20] Freitag T. E., Toet S., Ineson P., . Links between Methane Flux and Transcriptional Activities of Methanogens and Methane Oxidizers in a Blanket Peat Bog. FEMS Microbiology Ecology, 2010, 73(1): 157-165.

[21] Gong L. F., Wang H. M., Xiang X., . pH Shaping the Composition of sqhC–Containing Bacterial Communities. Geomicrobiology Journal, 2015, 32(5): 433-444.

[22] Gougoulias C., Clark J. M., Shaw L. J. The Role of Soil Microbes in the Global Carbon Cycle: Tracking the Below–Ground Microbial Processing of Plant–Derived Carbon for Manipulating Carbon Dynamics in Agricultural Systems. Journal of the Science of Food and Agriculture, 2014, 94(12): 2362-2371.

[23] Grayston S. J., Campbell C. D., Bardgett R. D., . Assessing Shifts in Microbial Community Structure across a Range of Grasslands of Differing Management Intensity Using CLPP, PLFA and Community DNA Techniques. Applied Soil Ecology, 2004, 25(1): 63-84.

[24] Gryta A., Frac M., Oszust K. The Application of the Biolog EcoPlate Approach in Ecotoxicological Evaluation of Dairy Sewage Sludge. Applied Biochemistry and Biotechnology, 2014, 174(4): 1434-1443.

[25] Häder D. P., Sinha R. P. Solar Ultraviolet Radiation–Induced DNA Damage in Aquatic Organisms: Potential Environmental Impact. Fundamental and Molecular Mechanisms of Mutagenesis, 2005, 571(1/2): 221-233.

[26] Heitkamp M. A., Cerniglia C. E. Mineralization of Polycyclic Aromatic Hydrocarbons by a Bacterium Isolated from Sediment Below an Oil Field. Applied and Environmental Microbiology, 1988, 54(6): 1612-1614.

[27] Hijnen W. A. M., Beerendonk E. F., Medema G. J. Inactivation Credit of UVR adiation for Viruses, Bacteria and Protozoan (oo)Cysts in Water: A Review. Water Research, 2006, 40(1): 3-22.

[28] Huang X. F., Mu T. S., Shen C. M., . Effects of Bio–Surfactants Combined with Alkaline Conditions on Volatile Fatty Acid Production and Microbial Community in the Anaerobic Fermentation of Waste Activated Sludge. International Biodeterioration & Biodegradation, 2016, 114: 24-30.

[29] Huang X. Y., Wang C. F., Xue J. T., . Occurrence of Diploptene in Moss Species from the Dajiuhu Peatland in Southern China. Organic Geochemistry, 2010, 41(3): 321-324.

[30] Juottonen H., Hynninen A., Nieminen M., . Methane–Cycling Microbial Communities and Methane Emission in Natural and Restored Peatlands. Applied and Environmental Microbiology, 2012, 78(17): 6386-6389.

[31] Kirchman D. L., Morán X. A. G., Ducklow H. Microbial Growth in the Polar Oceans–Role of Temperature and Potential Impact of Climate Change. Nature Reviews Microbiology, 2009, 7(6): 451-459.

[32] Kong X., Wang C., Ji M. Analysis of Microbial Metabolic Characteristics in Mesophilic and Thermophilic Biofilters Using Biolog Plate Technique. Chemical Engineering Journal, 2013, 230(16): 415-421.

[33] Kourtev P. S., Hill K. A., Shepson P. B., . Atmospheric Cloud Water Contains a Diverse Bacterial Community. Atmospheric Environment, 2011, 45(30): 5399-5405.

[34] Litchfield C., Gillevet P. Microbial Diversity and Complexity in Hypersaline Environments: A Preliminary Assessment. Journal of Industrial Microbiology & Biotechnology, 2002, 28(1): 48-55.

[35] Loisel J. G., Sala A. V., Yu Z. Global–Scale Pattern of Peatland Sphagnum Growth Driven by Photosynthetically Active Radiation and Growing Season Length. Biogeosciences, 2012, 9(7): 2737-2746.

[36] Louis P., Scott K. P., Duncan S. H., . Understanding the Effects of Diet on Bacterial Metabolism in the Large Intestine. Journal of Applied Microbiology, 2007, 102(5): 1197-1208.

[37] Mikan C. J., Schimel J. P., Doyle A. P. Temperature Controls of Microbial Respiration in Arctic Tundra Soils above and below Freezing. Soil Biology and Biochemistry, 2002, 34(11): 1785-1795.

[38] Moore S., Evans C. D., Page S. E., . Deep Instability of Deforested Tropical Peatlands Revealed by Fluvial Organic Carbon Fluxes. Nature, 2013, 493(7434): 660-663.

[39] Moorhead D. L., Lashermes G., Sinsabaugh R. L. A Theoretical Model of C–and N–Acquiring Exoenzyme Activities, which Balances Microbial Demands during Decomposition. Soil Biology and Biochemistry, 2012, 53: 133-141.

[40] Myers R. T., Zak D. R., White D. C., . Landscape–Level Patterns of Microbial Community Composition and Substrate Use in Upland Forest Ecosystems. Soil Science Society of America Journal, 2001, 65(2): 359-367.

[41] Ridgwell A., Hargreaves J. C., Edwards N. R., . Marine Geochemical Data Assimilation in an Efficient Earth System Model of Global Biogeochemical Cycling. Biogeosciences, 2007, 4(1): 87-104.

[42] Rousk J., Bååth E., Brookes P. C., . Soil Bacterial and Fungal Communities across a pH Gradient in an Arable Soil. The ISME Journal, 2010, 4(10): 1340-1351.

[43] Sanz–Lázaro C., Valdemarsen T., Marín A., . Effect of Temperature on Biogeochemistry of Marine Organic–Enriched Systems: Implications in a Global Warming Scenario. Ecological Applications, 2011, 21(7): 2664-2677.

[44] Satoh H., Miura Y., Tsushima I., . Layered Structure of Bacterial and Archaeal Communities and Their in situ Activities in Anaerobic Granules. Applied and Environmental Microbiology, 2007, 73(22): 7300-7307.

[45] Tian J., McCormack L., Wang J. Y., . Linkages between the Soil Organic Matter Fractions and the Microbial Metabolic Functional Diversity within a Broad–Leaved Korean Pine Forest. European Journal of Soil Biology, 2015, 66: 57-64.

[46] Williams C. J., Yamashita Y., Wilson H. F., . Unraveling the Role of Land Use and Microbial Activity in Shaping Dissolved Organic Matter Characteristics in Stream Ecosystems. Limnology and Oceanography, 2010, 55(3): 1159-1171.

[47] Wong J. W. C., Lai K. M., Wan C. K., . Isolation and Optimization of PAH–Degradative Bacteria from Contaminated Soil for PAHs Bioremediation. Water, Air, and Soil Pollution, 2002, 139(1–4): 1-13.

[48] Xiang X., Wang H. M., Gong L. F., . Vertical Variations and Associated Ecological Function of Bacterial Communities from Sphagnum to Underlying Sediments in Dajiuhu Peatland. Science China Earth Sciences, 2014, 57(5): 1013-1020.

[49] Xiang X., Wang R. C., Wang H. M., . Distribution of Bathyarchaeota Communities across Different Terrestrial Settings and Their Potential Ecological Functions. Scientific Reports, 2017, 7 45028

[50] Xie Z. Y., Hu C. Q., Zhang L. P., . Identification and Pathogenicity of Vibrio Ponticus Affecting Cultured Japanese Sea Bass, Lateolabrax Japonicus (Cuvier in Cuvier and Valenciennes). Letters in Applied Microbiology, 2007, 45(1): 62-67.

[51] Zak D. R., Pregitzer K. S. Spatial and Temporal Variability of Nitrogen Cycling in Northern Lower Michigan. Forest Science, 1990, 36(2): 367-380.

[52] Zhang W., Parker K. M., Luo Y., . Soil Microbial Responses to Experimental Warming and Clipping in a Tallgrass Prairie. Global Change Biology, 2005, 11(2): 266-277.

[53] Zhang Y., Cao C., Guo L., . Soil Properties, Bacterial Community Composition, and Metabolic Diversity Responses to Soil Salinization of a Semiarid Grassland in Northeast China. Journal of Soil and Water Conservation, 2015, 70(2): 110-120.

[54] Zhao S. L., Guo Y., Sheng Q. H., . Advanced Heat Map and Clustering Analysis Using Heatmap3. BioMed Research International, 2014, 2014 986048.

[55] Zhao Y. G., Ren N. Q., Wang A. J. Contributions of Fermentative Acidogenic Bacteria and Sulfate–Reducing Bacteria to Lactate Degradation and Sulfate Reduction. Chemosphere, 2008, 72(2): 233-242.