Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-27T10:34:08.332Z Has data issue: false hasContentIssue false
  • English
  • Français

FLEXIBLE SOIL MICROBIAL CARBON METABOLISM ACROSS AN ASIAN ELEVATION GRADIENT

Published online by Cambridge University Press:  16 July 2021

Yishan Jiang ,
Dayi Zhang ,
Nicholas J Ostle ,
Chunling Luo Open the ORCID record for Chunling Luo [Opens in a new window] ,
Yan Wang ,
Ping Ding ,
Zhineng Cheng Open the ORCID record for Zhineng Cheng [Opens in a new window] ,
Chengde Shen  and
Gan Zhang
Yishan Jiang
Affiliation:
State Key Laboratory of Organic Geochemistry and Guangdong-Hong Kong-Macao Joint Laboratory for Environmental Pollution and Control, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou, 510640, China CAS Center for Excellence in Deep Earth Science, Guangzhou, 510640, China Academy of Green Manufacturing Engineering, Wuhan University of Science and Technology, Wuhan, 430081, China
Dayi Zhang
Affiliation:
School of Environment, Tsinghua University, Beijing, 100084, China
Nicholas J Ostle
Affiliation:
Lancaster Environment Centre, Lancaster University, Lancashire, LA14YQ, UK
Chunling Luo*
Affiliation:
State Key Laboratory of Organic Geochemistry and Guangdong-Hong Kong-Macao Joint Laboratory for Environmental Pollution and Control, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou, 510640, China CAS Center for Excellence in Deep Earth Science, Guangzhou, 510640, China College of Natural Resources and Environment, South China Agricultural University, Guangzhou, 510642, China
Yan Wang
Affiliation:
School of Environmental Science & Technology, Dalian University of Technology, Dalian, 116024, China
Ping Ding
Affiliation:
CAS Center for Excellence in Deep Earth Science, Guangzhou, 510640, China State Key Laboratory of Isotope Geochemistry, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou, 510640, China
Zhineng Cheng
Affiliation:
State Key Laboratory of Organic Geochemistry and Guangdong-Hong Kong-Macao Joint Laboratory for Environmental Pollution and Control, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou, 510640, China CAS Center for Excellence in Deep Earth Science, Guangzhou, 510640, China
Chengde Shen
Affiliation:
CAS Center for Excellence in Deep Earth Science, Guangzhou, 510640, China State Key Laboratory of Isotope Geochemistry, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou, 510640, China
Gan Zhang*
Affiliation:
State Key Laboratory of Organic Geochemistry and Guangdong-Hong Kong-Macao Joint Laboratory for Environmental Pollution and Control, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou, 510640, China CAS Center for Excellence in Deep Earth Science, Guangzhou, 510640, China
*
*Corresponding authors. Emails: clluo@gig.ac.cn, zhanggan@gig.ac.cn
*Corresponding authors. Emails: clluo@gig.ac.cn, zhanggan@gig.ac.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

The function and change of global soil carbon (C) reserves in natural ecosystems are key regulators of future carbon-climate coupling. Microbes play a critical role in soil carbon cycling and yet there is poor understanding of their roles and C metabolism flexibility in many ecosystems. We wanted to determine whether vegetation type and climate zone influence soil microbial community composition (fungi and bacteria) and carbon resource preference. We used a biomarker (phospholipid fatty acids, PLFAs), natural abundance 13C and 14C probing approach to measure soil microbial composition and C resource use, along a 1900–4167-m elevation gradient on Mount Gongga (7556 m asl), China. Mount Gongga has a vertical mean annual temperature gradient of 1.2–10.1°C and a diversity of typical vegetation zones in the Tibetan Plateau. Soils were sampled at 10 locations along the gradient capturing distinct vegetation types and climate zones from lowland subtropical-forest to alpine-meadow. PLFA results showed that microbial communities were composed of 2.1–51.7% bacteria and 2.0–23.2% fungi across the elevation gradient. Microbial biomass was higher and the ratio of soil fungi to bacteria (F/B) was lower in forest soils compared to meadow soils. δ13C varied between −33‰ to −17‰ with C3 plant carbon sources dominant across the gradient. Soil organic carbon (SOC) turnover did not vary among three soils we measured from three forest types (i.e., evergreen broadleaved subtropical, mixed temperate, coniferous alpine) and dissolved organic carbon (DOC) turnover decreased with soil elevation. Forest soil microbial PLFA 14C and δ13C measurements showed that forest type and climate were related to different microbial C use. The 14C values of microbial PLFAs i15, a15, 16:1, br17 decreased with elevation while those of C16:0, cyC17, and cyC19 did not show much difference among three forest ecosystems. Bacteria and bacillus represented by C16:1 and brC17 showed considerable microbial C metabolism flexibility and tended to use ancient carbon at higher altitudes. Anaerobes represented by cyC17 and cyC19 showed stronger C metabolism selectivity. Our findings reveal specific C source differences between and within soil microbial groups along elevation gradients.

Keywords

compound-specific 13Ccompound-specific 14Cindividual PLFAnatural ecosystemsoil C dynamic
Type
Research Article
Information
Radiocarbon , Volume 63 , Issue 5 , October 2021 , pp. 1397 - 1413
Check for updates
Copyright
© The Author(s), 2021. Published by Cambridge University Press for the Arizona Board of Regents on behalf of the University of Arizona

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abraham, WR, Hesse, C, Pelz, O. 1998. Ratios of carbon isotopes in microbial lipids as an indicator of substrate usage. Applied and Environmental Microbiology 64:4202–4209.CrossRefGoogle ScholarPubMed
Ahad, JME, Pakdel, H. 2013. Direct evaluation of in situ biodegradation in Athabasca oil sands tailings ponds using natural abundance radiocarbon. Environmental Science & Technology 47:10214–10222.Google ScholarPubMed
Balesdent, J, Mariotti, A, Guillet, B. 1987. Natural C-13 abundance as a tracer for studies of soil organic-matter dynamics. Soil Biology & Biochemistry 19:25–30.CrossRefGoogle Scholar
Boschker, HTS, Middelburg, JJ. 2002. Stable isotopes and biomarkers in microbial ecology. Fems Microbiology Ecology 40:85–95.CrossRefGoogle ScholarPubMed
Boschker, HTS, Nold, SC, Wellsbury, P, Bos, D, de Graaf, W, Pel, R, Parkes, RJ, Cappenberg, TE. 1998. Direct linking of microbial populations to specific biogeochemical processes by C-13-labelling of biomarkers. Nature 392:801–805.CrossRefGoogle Scholar
Burchuladze, AA, Chudý, M, Eristavi, IV, Pagava, SV, Povinec, P, Šivo, A, Togonidze, GI. 1989. Anthropogenic 14C variations in atmospheric CO2 and wines. Radiocarbon 31:771–776.CrossRefGoogle Scholar
Chen, QQ, Sun, YM, Shen, CD, Peng, SL, Yi, WX, Li, ZA, Jiang, MT. 2002. Organic matter turnover rates and CO flux from organic matter decomposition of mountain soil profiles in the subtropical area, south China. Catena 49:217–229.CrossRefGoogle Scholar
Cowie, BR, Greenberg, BM, Slater, GF. 2010. Determination of microbial carbon sources and cycling during remediation of petroleum hydrocarbon impacted soil using natural abundance C-14 analysis of PLFA. Environmental Science & Technology 44:2322–2327.CrossRefGoogle Scholar
Ding, P, Shen, CD, Wang, N, Yi, WX, Ding, XF, Fu, DP, Liu, KX, Zhou, LP. 2010. Turnover rate of soil organic matter and origin of soil (CO2)-C-14 in deep soil from a subtropical forest in Dinghushan biosphere reserve, south China. Radiocarbon 52:1422–1434.CrossRefGoogle Scholar
Eglinton, TI, Aluwihare, LI, Bauer, JE, Druffel, ERM, McNichol, AP. 1996. Gas chromatographic isolation of individual compounds from complex matrices for radiocarbon dating. Analytical Chemistry 68: 904–912.CrossRefGoogle ScholarPubMed
Eglinton, TI, Benitez Nelson, BC, Pearson, A, McNichol, AP, Bauer, JE, Druffel, ERM. 1997. Variability in radiocarbon ages of individual organic compounds from marine sediments. Science 277:796–799.CrossRefGoogle Scholar
Faure, G. 1978. Principles of isotope geology. Earth Science Reviews 14:190–191.Google Scholar
Fierer, N, Schimel, JP. 2003. A proposed mechanism for the pulse in carbon dioxide production commonly observed following the rapid rewetting of a dry soil. Soil Science Society of America Journal. 67:798–805.CrossRefGoogle Scholar
Filip, Z, Claus, H, Dippell, G. 1998. Degradation of humic substances by soil microorganisms—a review. Zeitschrift Fur Pflanzenernahrung Und Bodenkunde 161:605–612.CrossRefGoogle Scholar
Frostegård, Å, Bååth, E. 1996. The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biology and Fertility of Soils 22:59–65.CrossRefGoogle Scholar
Hagedorn, F, Gavazov, K, Alexander, JM. 2019. Above- and belowground linkages shape responses of mountain vegetation to climate change. Science 365:1119–1123.CrossRefGoogle ScholarPubMed
Hilasvuori, E, Akujarvi, A, Fritze, H, Karhu, K, Laiho, R, Makiranta, P, Oinonen, M, Palonen, V, Vanhala, P, Liski, J. 2013. Temperature sensitivity of decomposition in a peat profile. Soil Biology & Biochemistry 67:47–54.CrossRefGoogle Scholar
Hua, Q, Barbetti, M, Rakowski, AZ. 2013. Atmospheric radiocarbon for the period 1950–2010. Radiocarbon 55:2059–2072.CrossRefGoogle Scholar
Keinänen, MM, Martikainen, PJ, Korhonen, LK, Suutari, MH. 2003. Microbial community structure in biofilms and water of a drinking water distribution system determined by lipid biomarkers. Water Science & Technology A Journal of the International Association on Water Pollution Research 47:143–147.CrossRefGoogle ScholarPubMed
Kramer, C, Gleixner, G. 2006. Variable use of plant- and soil-derived carbon by microorganisms in agricultural soils. Soil Biology & Biochemistry 38:3267–3278.CrossRefGoogle Scholar
Kramer, C, Trumbore, S, Fröberg, M, Dozal, LMC, Zhang, DC, Xu, XM, Santos, GM, Hanson, PJ. 2010. Recent (<4 year old) leaf litter is not a major source of microbial carbon in a temperate forest mineral soil. Soil Biology & Biochemistry 42:1028–1037.CrossRefGoogle Scholar
Levin, I, Hesshaimer, V. 2000. Radiocarbon—a unique tracer of global carbon cycle dynamics. Radiocarbon 42:69–80.CrossRefGoogle Scholar
Levin, I, Kromer, B. 1997. Twenty years of atmospheric 14CO2 observations at Schauinsland Station, Germany. Radiocarbon 39(2):205–218.CrossRefGoogle Scholar
Li, JZ, Wang, GA, Liu, XZ. 2009. Variations in carbon isotope ratios of C3 plants and distribution of C4 plants along an altitudinal transect on the eastern slope of Mount Gongga. Science in China. Series D, Earth Sciences 39:1387–1396.Google Scholar
Liang, C, Balser, TC. 2011. Microbial production of recalcitrant organic matter in global soils: Implications for productivity and climate policy. Nature Reviews Microbiology 9(75):75.CrossRefGoogle ScholarPubMed
Mahmoudi, N, Porter, TM, Zimmerman, AR, Fulthorpe, RR, Kasozi, GN, Silliman, BR, Slater, GF. 2013. Rapid degradation of Deepwater Horizon spilled oil by indigenous microbial communities in Louisiana saltmarsh sediments. Environmental Science & Technology 47:13303–13312.CrossRefGoogle ScholarPubMed
Mambelli, S, Bird, JA, Gleixner, G, Dawson, TE, Torn, MS. 2011. Relative contribution of foliar and fine root pine litter to the molecular composition of soil organic matter after in situ degradation. Organic Geochemistry 42:1099–1108.Google Scholar
Mandalakis, M, Gustafsson, O. 2003. Optimization of a preparative capillary gas chromatography-mass spectrometry system for the isolation and harvesting of individual polycyclic aromatic hydrocarbons. Journal of Chromatography A 996:163–172.CrossRefGoogle ScholarPubMed
Mendez-Millan, M, Nguyen Tu, TT, Balesdent, J, Derenne, S, Derrien, D, Egasse, C, Thongo M’Bou, A, Zeller, B, Hatte, C. 2014. Compound-specific C-13 and C-14 measurements improve the understanding of soil organic matter dynamics. Biogeochemistry 118:205–223.CrossRefGoogle Scholar
Mills, CT, Slater, GF, Dias, RF, Carr, SA, Reddy, CM, Schmidt, R, Mandernack, KW. 2013. The relative contribution of methanotrophs to microbial communities and carbon cycling in soil overlying a coal-bed methane seep. Fems Microbiology Ecology 84:474–494.CrossRefGoogle ScholarPubMed
Nottingham, AT, Fierer, N, Turner, BL, Whitaker, J, Ostle, NJ, McNamara, NP, Bardgett, RD, Leff, JW, Salinas, N, Silman, MR, et. al. 2018. Microbes follow Humboldt:temperature drives plant and soil microbial diversity patterns from the Amazon to the Andes. Ecology 99:2455–2466.CrossRefGoogle ScholarPubMed
Pelz, O, Chatzinotas, A, Andersen, N, Bernasconi, SM, Hesse, C, Abraham, WR, Zeyer, J. 2001. Use of isotopic and molecular techniques to link toluene degradation in denitrifying aquifer microcosms to specific microbial populations. Archives of Microbiology 175:270–281.CrossRefGoogle ScholarPubMed
Rethemeyer, J, Kramer, C, Gleixner, G, Wiesenberg, GLB, Schwark, L, Andersen, N, Nadeau, MJ, Grootes, PM. 2004. Complexity of soil organic matter: AMS 14C analysis of soil lipid fractions and individual compounds. Radiocarbon 46:465–473.CrossRefGoogle Scholar
Rethemeyer, J, Kramer, C, Gleixner, G, John, B, Yamashita, T, Flessa, H, Andersen, N, Nadeau, MJ, Grootes, PM. 2005. Transformation of organic matter in agricultural soils: radiocarbon concentration versus soil depth. Geoderma 128:94–105.CrossRefGoogle Scholar
Reimer, PJ, Brown, TA, Reimer, RW. 2004. Discussion: reporting and calibration of post-bomb C-14 data. Radiocarbon 46:1299–1304.Google Scholar
Sage, RF, Sage, TL. 2002. Microsite characteristics of Muhlenbergia richardsonis (Trin.) Rydb., an alpine C4 grass from the White Mountains, California. Oecologia 132:501–508.CrossRefGoogle ScholarPubMed
Schaeffer, SM, Ziegler, SE, Belnap, J, Evans, RD. 2012. Effects of Bromus tectorum invasion on microbial carbon and nitrogen cycling in two adjacent undisturbed arid grassland communities. Biogeochemistry 111:427–441.CrossRefGoogle Scholar
Schwab, VF, Nowak, ME, Elder, CD, Trumbore, SE, Xu, X, Gleixner, G, Lehmann, R, Pohnert, G, Muhr, J, Küsel, K, Totsche, KU. 2019. 14C-free carbon is a major contributor to cellular biomass in geochemically distinct groundwater of shallow sedimentary bedrock aquifers. Water Resources Research 55:2104–2121.CrossRefGoogle ScholarPubMed
Slater, GF, White, HK, Eglinton, TI, Reddy, CM. 2005. Determination of microbial carbon sources in petroleum contaminated sediments using molecular C-14 analysis. Environmental Science & Technology 39:2552–2558.CrossRefGoogle Scholar
Slater, GF, Nelson, RK, Kile, BM, Reddy, CM. 2006. Intrinsic bacterial biodegradation of petroleum contamination demonstrated in situ using natural abundance, molecular-level C-14 analysis. Organic Geochemistry 37:981–989.CrossRefGoogle Scholar
Smith, AP, Marín-Spiotta, E, Graaff, MAD, Balser, TC. 2014. Microbial community structure varies across soil organic matter aggregate pools during tropical land cover change. Soil Biology & Biochemistry 77:292–303.CrossRefGoogle Scholar
Song, MK. 1987. The climate characters of the Gong-ga mountain. Exploration of Nature 6:145–148.Google Scholar
Stuiver, M, Polach, HA. 1977. Reporting of C-14 data: discussion. Radiocarbon 19:355–363.CrossRefGoogle Scholar
Su, PX, Xie, TT, Zhou, ZJ. 2011. Geographical distribution of C4 plant species in desert regions of China and its relation with climate factors. Journal of Desert Research 31:267–276.Google Scholar
Stuiver, M, Polach, HA. 2006. Discussion: reporting of 14C data. Journal of Biological Chemistry 287:4726–4739.Google Scholar
Strauss, SL, Garcia-Pichel, F, Day, TA. 2012. Soil microbial carbon and nitrogen transformations at a glacial foreland on Anvers Island, Antarctic Peninsula. Polar Biology 35:1459–1471.CrossRefGoogle Scholar
Thomas, A. 1997. The climate of the Gongga Shan range, Sichuan Province, PR China. Arctic and Alpine Research 29:226–232.CrossRefGoogle Scholar
Trumbore, SE. 2000. Age of soil organic matter and soil respiration: radiocarbon constraints on belowground C dynamics. Ecological Applications 10:399–411.CrossRefGoogle Scholar
Trumbore, SE. 2009. Radiocarbon and soil carbon dynamics. Annual Review of Earth and Planetary Sciences 37:47–66.CrossRefGoogle Scholar
Uchida, M, Shibata, Y, Kawamura, K, Yoneda, M, Mukai, H, Tanaka, A, Uehiro, T, Morita, M. 2000. Isolation of individual fatty acids in sediments using preparative capillary gas chromatography (PCGC) for radiocarbon analysis at NIES-TERRA. Nuclear Instruments & Methods in Physics Research Section B 172:583–588.CrossRefGoogle Scholar
Wang, GA, Han, JM, Zhou, LP, Xiong, XG, Wu, ZH. 2005a. Carbon isotope ratios of plants and occurrences of C4 species under different soil moisture regimes in arid region of Northwest China. Physiologia Plantarum 125:74–81.CrossRefGoogle Scholar
Wang, HY, Nie, Y, Butterly, CR, Wang, L, Chen, QH, Tian, W, Song, BB, Xi, YG, Wang, Y. 2017. Fertilization alters microbial community composition and functional patterns by changing the chemical nature of soil organic carbon: a field study in a Halosol. Geoderma 292:17–24.CrossRefGoogle Scholar
Wang, L, Iv, HY, Wu, NQ, Chu, D, Han, JM, Wu, YH, Wu, HB, Gu, ZY. 2004a. Found of C4 plants in high elevation area of Tibet Plateau. Chinese Science Bulletin 49:1290–1293.Google Scholar
Wang, L, Ouyang, H, Zhou, CP, Zhang, F, Bai, JH, Peng, K. 2004b. Distribution characteristics of soil organic matter and nitrogen on the eastern slope of Mt. Gongga. Acta Geographica Sinica 59:1012–1019.Google Scholar
Wang, L, Ouyang, H, Zhou, CP, Zhang, F, Song, MH, Tian, YQ. 2005b. Soil organic matter dynamics along a vertical vegetation gradient in the Mount Gongga on the Tibetan Plateau. Journal of Integrative Plant Biology 47:411–420.CrossRefGoogle Scholar
Werner, RA, Brand, WA. 2001. Referencing strategies and techniques in stable isotope ratio analysis. Rapid Communications in Mass Spectrometry. 15:501–519.CrossRefGoogle ScholarPubMed
Whitaker, J, Ostle, N, McNamara, NP, Nottingham, AT, Stott, AW, Bardgett, RD, Salinas, N, Ccahuana, AJQ, Meir, P. 2014. Microbial carbon mineralization in tropical lowland and montane forest soils of Peru. Frontiers in Microbiology 5:13.CrossRefGoogle ScholarPubMed
White, DC, Davis, WM, Nickels, JS, King, JD, Bobbie, RJ. 1979. Determination of the sedimentary microbial biomass by extractable lipid phosphate. Oecologia 40:51–62.CrossRefGoogle Scholar
Wu, YH, Li, W, Zhou, J, Cao, Y. 2013. Temperature and precipitation variations at two meteorological stations on eastern slope of Gongga Mountain, SW China in the past two decades. Journal of Mountain Science 10:370–377.CrossRefGoogle Scholar
Xu, M, Li, XL, Cai, XB, Gai, JP, Li, XL, Christie, P, Zhang, JL. 2014. Soil microbial community structure and activity along a montane elevational gradient on the Tibetan Plateau. European Journal of Soil Biology 64:6–14.CrossRefGoogle Scholar
Yang, H, Lu, Q, Wu, B, Yang, H, Zhang, J, Lin, Y. 2006. Vegetation diversity and its application in sandy desert revegetation on Tibetan Plateau. Journal of Arid Environments 65:619–631.CrossRefGoogle Scholar
Yevdokimov, IV, Larionova, AA, Stulin, AF. 2013. Turnover of “new” and “old” carbon in soil microbial biomass. Microbiology 82:505–516.CrossRefGoogle Scholar
Zelles, L, Bai, QY, Rackwitz, R, Chadwick, D, Beese, F. 1995. Determination of phospholipid-derived and lipopolysaccharide-derived fatty-acids as an estimate of microbial biomass and community structures in soils. Biology and Fertility of Soils 19:115–123.CrossRefGoogle Scholar
Zhang, DC, Xu, XM, Aziolkowski, L, Rsouthon, J, Santos, GM, Etrumbore, S. 2010. Compound-specific radiocarbon analyses of phospholipid fatty acids and N-Alkanes in ocean sediments. Radiocarbon 52:1215–1223.Google Scholar
Zhang, XY, Zhao, L, Wang, YX, Xu, YP, Zhou, LP. 2013. Optimization of programmed-temperature vaporization injection preparative capillary GC for compound specific radiocarbon analysis. Journal of Separation Science 36:2136–2144.CrossRefGoogle ScholarPubMed
Zhong, XH, Zhang, WJ, Luo, Y. 1999. The characteristics of the mountain ecosystem and environment in the Mount Gongga region. AMBIO-A Journal of the Human Environment 28:648–654.Google Scholar
Ziegler, SE, Billings, SA, Lane, CS, Jianwei, L, Fogel, ML. 2013. Warming alters routing of labile and slower-turnover carbon through distinct microbial groups in boreal forest organic soils. Soil Biology & Biochemistry 60:23–32.CrossRefGoogle Scholar
Ziolkowski, LA, Wierzchos, J, Davila, AF, Slater, GF. 2013. Radiocarbon evidence of active endolithic microbial communities in the hyperarid core of the Atacama desert. Astrobiology 13:607–616.CrossRefGoogle ScholarPubMed
Supplementary material: File

Jiang et al. supplementary material

Jiang et al. supplementary material

Download Jiang et al. supplementary material(File)
File 875.2 KB