Advertisement

Biogeochemistry

, Volume 124, Issue 1–3, pp 13–26 | Cite as

Distinct fungal and bacterial δ13C signatures as potential drivers of increasing δ13C of soil organic matter with depth

  • Lukas Kohl
  • Jérôme Laganière
  • Kate A. Edwards
  • Sharon A. Billings
  • Penny L. Morrill
  • Geert Van Biesen
  • Susan E. Ziegler
Biogeochemistry Letters
First Online:
Received:
Accepted:

Abstract

Soil microbial biomass is a key source of soil organic carbon (SOC), and the increasing proportion of microbially derived SOC is thought to drive the enrichment of 13C during SOC decomposition. Yet, little is known about how the δ13C of soil microbial biomass differs across space or time, or with the composition of the microbial community. Variation in soil microbial δ13C may occur due to variation in substrates used by soil microorganisms, and variation in how different microorganisms synthesize biomass. Understanding these variations in soil microbial δ13C would enable more accurate interpretation of patterns in the δ13C of SOC. Here, we report the variation in δ13C values of individual phospholipid fatty acids (PLFA) within podzolic soils from mesic boreal forests characterized by steep decreases in fungal to bacterial (F:B) ratios. By comparing trends in δ13C of PLFA indicative of either fungi or bacteria to those PLFA common across both microbial groups, we tested the hypothesis that the enrichment of 13C in bacterial relative to fungal biomass represents a mechanism for the increase of bulk SOC δ13C with depth. We demonstrate that PLFA derived from fungi were consistently depleted in 13C (−40.1 to −30.6 ‰) relative to those derived from bacteria (−31.1 to −24.6  ‰), but unlike bulk SOC the δ13C of PLFA from either group did not vary significantly with depth. In contrast, the δ13C of PLFA produced by both fungi and bacteria, which represent the δ13C of soil microbial biomass as a whole, strongly increased with depth (increase of 7.6–8.4 ‰) and was negatively correlated with the fungi/(fungi + bacteria) ratio (R2 > 0.88). The steep increase of the δ13C of general PLFA with depth cannot be explained by an increase in the δ13C of either fungal or bacterial biomass alone since the PLFA indicative of those groups did not vary with depth. Instead, these data demonstrate that the increase in soil biomass δ13C with depth is driven by a change in the proportion of bacterial relative to fungal biomass. We suggest that the increased proportions of soil bacterial relative to fungal biomass with depth may represent an important mechanism contributing to increasing δ13CSOC with depth via contributions from ‘necromass’ to SOC.

Keywords

13C Necromass Podzols Soil organic carbon PLFA Soil microbial biomass 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

We thank Jamie Warren for laboratory assistance; Thalia Soucy-Giguère for help with field sampling; Birgit Wild, Lucia Fuchslueger, Frances Podrebarac, and Scarlett Vallaire for helpful conversation and comments on the manuscript; and Frances Podrebarac for providing the soil profile pictures used in Fig. 1. We furthermore thank three anonymous reviewers who helped to substantially improve the manuscript. Our study was funded by the Natural Sciences and Engineering Research Council of Canada, the Center for Forestry Science and Innovation (Department of Natural Resources, Government of Newfoundland and Labrador), the Canada Research Chairs program, and the Humber River Basin Project (Government of Newfoundland and Labrador).

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

10533_2015_107_MOESM1_ESM.pdf (113 kb)
Supplementary material 1 (PDF 112 kb)
10533_2015_107_MOESM2_ESM.pdf (79 kb)
Supplementary material 2 (PDF 79 kb)
10533_2015_107_MOESM3_ESM.pdf (157 kb)
Supplementary material 3 (PDF 156 kb)
10533_2015_107_MOESM4_ESM.pdf (60 kb)
Supplementary material 4 (PDF 59 kb)
10533_2015_107_MOESM5_ESM.pdf (45 kb)
Supplementary material 5 (PDF 44 kb)
10533_2015_107_MOESM6_ESM.pdf (106 kb)
Supplementary material 6 (PDF 106 kb)
10533_2015_107_MOESM7_ESM.pdf (98 kb)
Supplementary material 7 (PDF 98 kb)
10533_2015_107_MOESM8_ESM.pdf (19 kb)
Supplementary material 8 (PDF 19 kb)

References

  1. Abraham W-R, Hesse C (2003) Isotope fractionations in the biosynthesis of cell components by different fungi: a basis for environmental carbon flux studies. FEMS Microbiol Ecol 46:121–128. doi: 10.1016/S0168-6496(03)00203-4 CrossRefGoogle Scholar
  2. Abraham W, Hesse C, Pelz O (1998) Ratios of carbon isotopes in microbial lipids as an indicator of substrate usage. Appl Environ Microbiol 64:4202–4209Google Scholar
  3. Abrajano TA, Murphy D, Fang J et al (1994) 13C/12C ratios in individual fatty acids of marine mytilids with and without bacterial symbionts. Org Geochem 21:611–617. doi: 10.1016/0146-6380(94)90007-8 CrossRefGoogle Scholar
  4. Baum C, Fienemann M, Glatzel S, Gleixner G (2009) Overstory-specific effects of litter fall on the microbial carbon turnover in a mature deciduous forest. For Ecol Manage 258:109–114. doi: 10.1016/j.foreco.2009.03.047 CrossRefGoogle Scholar
  5. Billings SA, Ziegler SE (2008) Altered patterns of soil carbon substrate usage and heterotrophic respiration in a pine forest with elevated CO2 and N fertilization. Glob Change Biol 14:1025–1036. doi: 10.1111/j.1365-2486.2008.01562.x CrossRefGoogle Scholar
  6. Bol R, Poirier N, Balesdent J, Gleixner G (2009) Molecular turnover time of soil organic matter in particle-size fractions of an arable soil. Rapid Commun Mass Spectrom 23:2551–2558. doi: 10.1002/rcm.4124 CrossRefGoogle Scholar
  7. Boström B, Comstedt D, Ekblad A (2007) Isotope fractionation and 13C enrichment in soil profiles during the decomposition of soil organic matter. Oecologia 153:89–98. doi: 10.1007/s00442-007-0700-8 CrossRefGoogle Scholar
  8. Bouillon S, Boschker HTS, Brussel VU (2006) Bacterial carbon sources in coastal sediments: a cross-system analysis based on stable isotope data of biomarkers. Biogeosciences 3:175–185CrossRefGoogle Scholar
  9. Churchland C, Grayston SJ, Bengtson P (2013) Spatial variability of soil fungal and bacterial abundance: consequences for carbon turnover along a transition from a forested to clear-cut site. Soil Biol Biochem 63:5–13. doi: 10.1016/j.soilbio.2013.03.015 CrossRefGoogle Scholar
  10. Cifuentes LA, Salata GG (2001) Signicance of carbon isotope discrimination between bulk carbon and extracted phospholipid fatty acids in selected terrestrial and marine environments. Org Geochem 32:613–621. doi: 10.1016/S0146-6380(00)00198-4 CrossRefGoogle Scholar
  11. Coffin R, Velinsky D, Devereux R et al (1990) Stable carbon isotope analysis of nucleic acids to trace sources of dissolved substrates used by estuarine bacteria. Appl Environ Microbiol 56:2012–2020Google Scholar
  12. Cusack DF, Silver WL, Torn MS et al (2011) Changes in microbial community characteristics and soil organic matter with nitrogen additions in two tropical forests. Ecology 92:621–632. doi: 10.1890/10-0459.1 CrossRefGoogle Scholar
  13. DeNiro MJ, Epstein S (1977) Mechanism of carbon isotope fractionation associated with lipid synthesis. Science 197:261–263. doi: 10.1126/science.327543 CrossRefGoogle Scholar
  14. Dijkstra P, Ishizu A, Doucett R et al (2006) 13C and 15N natural abundance of the soil microbial biomass. Soil Biol Biochem 38:3257–3266. doi: 10.1016/j.soilbio.2006.04.005 CrossRefGoogle Scholar
  15. Ehleringer J, Schulze E, Ziegler H et al (1985) Xylem-tapping mistletoes: water or nutrient parasites. Science 227(80):1479–1481. doi: 10.1126/science.227.4693.1479 CrossRefGoogle Scholar
  16. Ehleringer J, Buchmann N, Flanagan L (2000) Carbon isotope ratios in belowground carbon cycle processes. Ecol Appl 10:412–422. doi: 10.1890/1051-0761(2000)010[0412:CIRIBC]2.0.CO;2
  17. Esperschütz J, Pérez-de-Mora A, Schreiner K et al (2011) Microbial food web dynamics along a soil chronosequence of a glacier forefield. Biogeosciences 8:3283–3294. doi: 10.5194/bg-8-3283-2011 CrossRefGoogle Scholar
  18. Frostegård Å, Tunlid A, Bååth E (2010) Use and misuse of PLFA measurements in soils. Soil Biol Biochem 43:1621–1625. doi: 10.1016/j.soilbio.2010.11.021 CrossRefGoogle Scholar
  19. Fry B, Joern A, Parker P (1978) Grasshopper food web analysis: use of carbon isotope ratios to examine feeding relationships among terrestrial herbivores. Ecology 59:498–506. doi: 10.2307/1936580 CrossRefGoogle Scholar
  20. Glaser B, Amelung W (2002) Determination of 13C natural abundance of amino acid enantiomers in soil: methodological considerations and first results. Rapid Commun Mass Spectrom 16:891–898. doi: 10.1002/rcm.650
  21. Gleixner G, Danier HJ, Werner RA, Schmidt HL (1993) Correlations between the 13C content of primary and secondary plant products in different cell compartments and that in decomposing basidiomycetes. Plant Physiol 102:1287–1290. doi: 10.1104/pp.102.4.1287 Google Scholar
  22. Grandy SA, Neff JC (2008) Molecular C dynamics downstream: the biochemical decomposition sequence and its impact on soil organic matter structure and function. Sci Total Environ 404:297–307. doi: 10.1016/j.scitotenv.2007.11.013 CrossRefGoogle Scholar
  23. Grogan DW, Cronan JE (1997) Cyclopropane ring formation in membrane lipids of bacteria. Microbiol Mol Biol Rev 61:429–441Google Scholar
  24. Hayes J (1993) Factors controlling 13C contents of sedimentary organic compounds: principles and evidence. Mar Geol 113:111–125. doi: 10.1016/0025-3227(93)90153-M CrossRefGoogle Scholar
  25. Hayes JM (2001) Fractionation of carbon and hydrogen isotopes in biosynthetic processes. In: Valley JW, Cole DR (eds) Reviews in mineralogy and geochemistry. Mineralogical Society of America, Washington, pp 225–277Google Scholar
  26. Hayes JM, Freeman KH, Popp BN, Hoham CH (1990) Compound-specific isotopic analyses: a novel tool for reconstruction of ancient biogeochemical processes. Org Geochem 16:1115–1128. doi: 10.1016/0146-6380(90)90147-R CrossRefGoogle Scholar
  27. Hobbie E, Werner R (2004) Intramolecular, compound-specific, and bulk carbon isotope patterns in C3 and C4 plants: a review and synthesis. New Phytol 161:371–385. doi: 10.1046/j.1469-8137.2004.00970.x CrossRefGoogle Scholar
  28. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363. doi: 10.1002/bimj.200810425 CrossRefGoogle Scholar
  29. Kramer C, Gleixner G (2006) Variable use of plant- and soil-derived carbon by microorganisms in agricultural soils. Soil Biol Biochem 38:3267–3278. doi: 10.1016/j.soilbio.2006.04.006 CrossRefGoogle Scholar
  30. Laganière J, Billings SA, Edwards K et al (2015) A warmer climate induces reduced bioreactivity of isolated boreal forest soil horizons without increasing the temperature sensitivity of CO2 respiratory losses. Soil Biol Biochem (in press)Google Scholar
  31. Macko SA, Estep MLF (1984) Microbial alteration of stable nitrogen and carbon isotopic compositions of organic matter. Org Geochem 6:787–790. doi: 10.1016/0146-6380(84)90100-1 CrossRefGoogle Scholar
  32. Miltner A, Kindler R, Knicker H et al (2009) Fate of bacterial biomass derived fatty acids in soil and their contribution to soil organic matter. Org Geochem 40:978–985. doi: 10.1016/j.orggeochem.2009.06.008 CrossRefGoogle Scholar
  33. Miltner A, Bombach P, Schmidt-Brücken B, Kästner M (2011) SOM genesis: microbial biomass as a significant source. Biogeochemistry 111:41–55. doi: 10.1007/s10533-011-9658-z CrossRefGoogle Scholar
  34. Nadelhoffer K, Fry B (1988) Controls on natural nitrogen-15 and carbon-13 abundances in forest soil organic matter. Soil Sci Soc Am J 52:1633–1640. doi: 10.2136/sssaj1988.03615995005200060024x CrossRefGoogle Scholar
  35. Nakamura K, Takai Y, Wada E (1990) Carbon isotopes of soil gases and related organic matter in an agroecosystem with special reference to paddy field. In: Durrance EM, Galimov EM, Hinkle ME et al (eds) Geochemistry of gaseous elements and compounds. Theophrastus Publications, Athens, pp 455–484Google Scholar
  36. Osono T (2007) Ecology of ligninolytic fungi associated with leaf litter decomposition. Ecol Res 22:955–974. doi: 10.1007/s11284-007-0390-z CrossRefGoogle Scholar
  37. Peterson BJ, Howarth RW, Garritt RH (1985) Multiple stable isotopes used to trace the flow of organic matter in estuarine food webs. Science 227(80):1361–1363. doi: 10.1126/science.227.4692.1361 CrossRefGoogle Scholar
  38. Phillips CL, McFarlane KJ, Risk D, Desai AR (2013) Biological and physical influences on soil 14CO2 seasonal dynamics in a temperate hardwood forest. Biogeosciences 10:7999–8012. doi: 10.5194/bg-10-7999-2013 CrossRefGoogle Scholar
  39. Rinnan R, Bååth E (2009) Differential utilization of carbon substrates by bacteria and fungi in tundra soil. Appl Environ Microbiol 75:3611–3620. doi: 10.1128/AEM.02865-08 CrossRefGoogle Scholar
  40. Ruess L, Chamberlain PM (2010) The fat that matters: soil food web analysis using fatty acids and their carbon stable isotope signature. Soil Biol Biochem 42:1898–1910. doi: 10.1016/j.soilbio.2010.07.020 CrossRefGoogle Scholar
  41. Schimel JP, Schaeffer SM (2012) Microbial control over carbon cycling in soil. Front Microbiol 3:348. doi: 10.3389/fmicb.2012.00348 CrossRefGoogle Scholar
  42. Schlesinger W, Andrews J (2000) Soil respiration and the global carbon cycle. Biogeochemistry 48:7–20. doi: 10.1023/A%3A1006247623877 CrossRefGoogle Scholar
  43. Schnecker J, Wild B, Takriti M et al (2015) Microbial community composition shapes enzyme patterns in topsoil and subsoil horizons along a latitudinal transect in Western Siberia. Soil Biol Biochem 83:106–115. doi: 10.1016/j.soilbio.2015.01.016 CrossRefGoogle Scholar
  44. Silfer J, Engel M, Macko S, Jumeau E (1991) Stable carbon isotope analysis of amino acid enantiomers by conventional isotope ratio mass spectrometry and combined gas chromatography/isotope ratio mass. Anal Chem 63:370–374. doi: 10.1021/ac00004a014 CrossRefGoogle Scholar
  45. Streit K, Hagedorn F, Hiltbrunner D et al (2014) Soil warming alters microbial substrate use in alpine soils. Glob Change Biol 20:1–12. doi: 10.1111/gcb.12396 CrossRefGoogle Scholar
  46. Strickland MS, Rousk J (2010) Considering fungal:bacterial dominance in soils: methods, controls, and ecosystem implications. Soil Biol Biochem 42:1385–1395. doi: 10.1016/j.soilbio.2010.05.007 CrossRefGoogle Scholar
  47. Teece MA, Fogel ML, Dollhopf ME, Nealson KH (1999) Isotopic fractionation associated with biosynthesis of fatty acids by a marine bacterium under oxic and anoxic conditions. Org Geochem 30:1571–1579. doi: 10.1016/S0146-6380(99)00108-4 CrossRefGoogle Scholar
  48. Waldrop MP, Firestone MK (2004) Microbial community utilization of recalcitrant and simple carbon compounds: impact of oak-woodland plant communities. Oecologia 138:275–284. doi: 10.1007/s00442-003-1419-9 CrossRefGoogle Scholar
  49. Wallander H, Göransson H, Rosengren U (2004) Production, standing biomass and natural abundance of 15N and 13C in ectomycorrhizal mycelia collected at different soil depths in two forest types. Oecologia 139:89–97. doi: 10.1007/s00442-003-1477-z CrossRefGoogle Scholar
  50. Werth M, Kuzyakov Y (2010) 13C fractionation at the root–microorganisms–soil interface: a review and outlook for partitioning studies. Soil Biol Biochem 42:1372–1384. doi: 10.1016/j.soilbio.2010.04.009 CrossRefGoogle Scholar
  51. Ziegler SE, Billings SA, Lane CS et al (2013) Warming alters routing of labile and slower-turnover carbon through distinct microbial groups in boreal forest organic soils. Soil Biol Biochem 60:23–32. doi: 10.1016/j.soilbio.2013.01.001 CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  1. 1.Department of Earth SciencesMemorial UniversitySt. John’sCanada
  2. 2.Natural Resources Canada, Canadian Forest ServiceLaurentian Forestry CentreQuébecCanada
  3. 3.Natural Resources Canada, Canadian Forest ServiceAtlantic Forestry CentreCorner BrookCanada
  4. 4.Department of Ecology and Evolutionary Biology, Kansas Biological SurveyUniversity of KansasLawrenceUSA

Personalised recommendations