Skip to main content

Advertisement

SpringerLink
Log in

Microbial methane production is affected by secondary metabolites in the heartwood of living trees in upland forests

  • Original Article
  • Published:
Trees Aims and scope Submit manuscript

Abstract

Key message

This paper shows that CH4 produced in the heartwood of living trees in upland forests is of microbial origin, and that microbial CH4 production may be suppressed in the heartwood with more phenolic compounds than carbohydrates.

Abstract

Methane (CH4) is a potent greenhouse gas that exerts large effects on atmospheric chemistry and the global warming. Living trees in upland forests might contribute to the global CH4 emissions but the contribution is poorly understood and the mechanisms of CH4 production in their heartwood are not completely clear. Using gene sequencing and a series of laboratory incubations, this study addressed whether CH4 produced in the heartwood of living trees in upland forests is microbial in origin and how the CH4 production is affected by secondary metabolites. Both the response of CH4 production to temperatures and the presence of methanogenic archaea indicate that the CH4 produced in heartwood was microbial in origin. Methanobacterium was the dominant methanogens in the heartwood of Populus canadensis which had high concentrations of CH4, and was absent from the heartwood of Pinus tabuliformis and Salix matsudana which produced negligible or very low CH4. Water- and ethanol-soluble extractives enhanced microbial CH4 production in heartwood incubations but acetone-soluble extractives inhibited the production. Since acetone-soluble extractives inhibited the production of microbial CH4, it is assumed that the CH4 production may be suppressed from heartwood with phenolic compounds that act as an antibiotic for methanogenic archaea in most living trees in upland forests. The inhibitory effects of secondary metabolites on microbial CH4 production in heartwood reduce the CH4 emissions from the stems of living trees in upland forests.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Angel R, Claus P, Conrad R (2012) Methanogenic archaea are globally ubiquitous in aerated soils and become active under wet anoxic conditions. ISME J 6:847–862

    Article  CAS  Google Scholar 

  • Balch WE, Fox GE, Magrum LJ, Woese CR, Wolfe RS (1979) Methanogens—re-evaluation of a unique biological group. Microbiol Rev 43:260–296

    CAS  PubMed  PubMed Central  Google Scholar 

  • Barba J et al (2019) Methane emissions from tree stems: a new frontier in the global carbon cycle. New Phytol. https://doi.org/10.1111/nph.15582

    Article  PubMed  Google Scholar 

  • Berry JA, Raison JK (1981) Responses of macrophytes to temperature. In: Lange OL, Nobel PS, Osmond CB, Ziegler H (eds) Physiological plant ecology I. Responses to the physical environment, Encyclopedia of Plant Physiology, New Series vol 12A. Spriner, Berlin, pp 277–338

    Google Scholar 

  • Bhattacharya A, Sood P, Citovsky V (2010) The roles of plant phenolics in defence and communication during Agrobacterium and Rhizobium infection. Mol Plant Pathol 11:705–719

    CAS  PubMed  PubMed Central  Google Scholar 

  • Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54:519–549

    Article  CAS  Google Scholar 

  • Chen ZJ, Zhou XY, Geng SC, Miao Y, Cao YH, Chen Z, Zhang JH, Han SJ (2019) Interactive effect of nitrogen addition and throughfall reduction decreases soil aggregate stability through reducing biological binding agents. For Ecol Manag 445:13–19

    Article  Google Scholar 

  • Cieslak A, Zmora P, Matkowski A, Nawrot-Hadzik I, Pers-Kamczyc E, El-Sherbiny M, Bryszak M, Szumacher-Strabel M (2016) Tannins from Sanguisorba officinalis affect in vitro rumen methane production and fermentation. J Anim Plant Sci 26:54–62

    CAS  Google Scholar 

  • Conrad R, Klose M, Noll M, Kemnitz D, Bodelier PLE (2008) Soil type links microbial colonization of rice roots to methane emission. Global Change Biol 14:657–669

    Article  Google Scholar 

  • Covey KR, Megonigal JP (2019) Methane production and emissions in trees and forests. New Phytol 222:35–51

    Article  Google Scholar 

  • Covey KR, Wood SA, Warren RJ, Lee X, Bradford MA (2012) Elevated methane concentrations in trees of an upland forest. Geophys Res Lett 39:L15705

    Article  Google Scholar 

  • Dunfield P, Knowles R, Dumont R, Moore TR (1993) Methane production and consumption in temperature and subarctic peat soils: response to temperature and pH. Soil Biol Biochem 25:321–326

    Article  CAS  Google Scholar 

  • FAO (Food and Agriculture Organization of the United Nations) (2010) Global Forest Resources Assessment 2010. For. pap. 163. FAO, Rome

    Google Scholar 

  • Gu Q, Chang SX, Wang ZP, Feng JC, Chen QS, Han XG (2016) Microbial versus non-microbial methane releases from fresh soils at different temperatures. Geoderma 284:178–184. https://doi.org/10.1016/j.geoderma.2016.08.027

    Article  CAS  Google Scholar 

  • Hristov AN, Oh J, Giallongo F, Frederick TW, Harper MT, Weeks HL, Branco AF, Moate PJ, Deighton MH, Williams SRO, Kindermann M, Duval S (2015) An inhibitor persistently decreased enteric methane emission from dairy cows with no negative effect on milk production. PNAS 112:10663–10668

    Article  CAS  Google Scholar 

  • Jiang YG, Yuan X, Zhang JH, Han SJ, Chen ZJ, Wang XG, Wang JW, Hao L, Li GD, Dong SZ, He HS (2019) Reconstruction of June–July temperatures based on a 233 year tree-ring of Picea jezoensis var. microsperma. Forests 10:416. https://doi.org/10.3390/f10050416

    Article  Google Scholar 

  • Jugold A, Althoff F, Hurkuck M, Greule M, Lenhart K, Lelieveld J, Keppler F (2012) Non-microbial methane formation in oxic soils. Biogeosciences 9:5291–5301

    Article  CAS  Google Scholar 

  • Keppler F, Hamilton JT, Brass M, Rockmann T (2006) Methane emissions from terrestrial plants under aerobic conditions. Nature 439:187–191

    Article  CAS  Google Scholar 

  • Kurth EF (1939) Separation of wood extractives into simpler components. Ind Eng Chem Anal 11:203–205

    Article  CAS  Google Scholar 

  • Liu H, Wang J, Wang A, Chen J (2011) Chemical inhibitors of methanogenesis and putative applications. Appl Microbiol Biotechnol 89:1333–1340

    Article  CAS  Google Scholar 

  • Luton PE, Wayne JM, Sharp RJ, Riley PW (2002) The mcrA gene as an alternative to 16S rRNA in the phylogenetic analysis of methanogen populations in landfill. Microbiology 148:3521–3530

    Article  CAS  Google Scholar 

  • Machacova K, Bäck J, Vanhatalo A, Halmeenmäki E, Kolari P, Mammarella I, Pumpanen J, Acosta M, Urban O, Pihlatie M (2016) Pinus sylvestris as a missing source of nitrous oxide and methane in boreal forest. Sci Rep 6:23410. https://doi.org/10.1038/srep23410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mink R, Dugan PR (1980) Microbial production of methane from wood and inhibition by ethanol extracts of wood. Ohio J Sci 80:242–249

    CAS  Google Scholar 

  • Pangala SR, Moore S, Hornibrook ERC, Gauci V (2013) Trees are major conduits for methane egress from tropical forested wetlands. New Phytol 197:524–531. https://doi.org/10.1111/nph.12031

    Article  PubMed  Google Scholar 

  • Pathak AK, Dutta N, Pattanaik AK, Chaturvedi VB, Sharma K (2017) Effect of condensed tannins from Ficus infectoria and Psidium guajava leaf meal mixture on nutrient metabolism, methane emission and performance of lambs. Asian Aust J Anim Sci 30:1702–1710

    Article  CAS  Google Scholar 

  • Patra AK (2010) Meta-analysis of effects of phytochemicals on digestibility and rumen fermentation characteristics associated with methanogenesis. J Sci Food Agric 90:2700–2708

    Article  CAS  Google Scholar 

  • Pitz SL, Megonigal JP (2017) Temperate forest methane sink diminished by tree emissions. New Phytol 214:1432–1439. https://doi.org/10.1111/nph.14559

    Article  CAS  PubMed  Google Scholar 

  • Pitz SL, Megonigal JP, Chang CH, Szlavecz K (2018) Methane fluxes from tree stems and soils along a habitat gradient. Biogeochemistry 137:307–320. https://doi.org/10.1007/s10533-017-0400-3

    Article  CAS  Google Scholar 

  • Plain C, Ndiaye F-K, Bonnaud P, Ranger J, Epron D (2018) Impact of vegetation on the methane budget of a temperate forest. New Phytol. https://doi.org/10.1111/nph.15452

    Article  PubMed  Google Scholar 

  • SAS Institute (1999) SAS/STATTM User’s Guide Release 8.0 Edition. SAS Institute Inc, Cary

    Google Scholar 

  • Wang ZP, Gulledge J, Zheng JQ, Liu W, Li LH, Han XG (2009) Physical injury stimulates aerobic methane emissions from terrestrial plants. Biogeosciences 6:615–621

    Article  CAS  Google Scholar 

  • Wang ZP, Chang SX, Chen H, Han XG (2013) Widespread non-microbial methane production by organic compounds and the impact of environmental stresses. Earth Sci Rev 127:193–202

    Article  CAS  Google Scholar 

  • Wang L, Cheng YN, Dan NH, Dan WH (2015) The extraction and purification methods of vegetable tannin and their development. West Leather 37:12–19

    Google Scholar 

  • Wang ZP, Gu Q, Deng FD, Huang JH, Megonigal JP, Yu Q, Lü XT, Li LH, Chang S, Zhang YH, Feng JC, Han XG (2016) Methane emissions from the trunks of living trees on upland soils. New Phytol 211:429–439. https://doi.org/10.1111/nph.13909

    Article  CAS  PubMed  Google Scholar 

  • Wang ZP, Han SJ, Li HL, Deng FD, Zheng YH, Liu HF, Han XG (2017) Methane production explained largely by water content in the heartwood of living trees in upland forests. J Geophys Res Biogeosci 122:2479–2489. https://doi.org/10.1002/2017JG003991

    Article  CAS  Google Scholar 

  • Wang AY, Han SJ, Zhang JH, Wang M, Yin XH, Fang LD, Yang D, Hao GY (2018) The interaction between nonstructural carbohydrate reserves and xylem hydraulics in Korean pine trees across an altitudinal gradient. Tree Physiol 38:1792–1804

    Article  CAS  Google Scholar 

  • Warner DL, Villarreal S, McWilliams K, Inamdar S, Vargas R (2017) Carbon dioxide and methane fluxes from tree stems, coarse woody debris, and soils in an upland temperate forest. Ecosystems. https://doi.org/10.1007/s10021-016-0106-8

    Article  Google Scholar 

  • Welch B, Gauci V, Sayer EJ (2019) Tree stem bases are sources of CH4 and N2O in a tropical forest on upland soil during the dry to wet season transition. Global Change Biol. https://doi.org/10.1111/gcb.14498

    Article  Google Scholar 

  • Wikandari R, Sari NK, A’Yun Q, Millati R, Cahyanto MN, Niklasson C, Taherzadeh MJ (2015) Effects of lactone, ketone, and phenolic compounds on methane production and metabolic intermediates during anaerobic digestion. Appl Biochem Biotechnol 175:1651–1663

    Article  CAS  Google Scholar 

  • Williams CM, Eun JS, MacAdam JW, Young AJ, Fellner V, Min BR (2011) Effects of forage legumes containing condensed tannins on methane and ammonia production in continuous cultures of mixed ruminal microorganisms. Anim Feed Sci Technol 166–167:364–372

    Article  Google Scholar 

  • Wu Y, Wang Q, Wang H, Wang W, Han S (2019) Shelterbelt poplar forests induced soil changes in deep soil profiles and climates contributed their inter-site variations in dryland regions, northeastern China. Front Plant Sci 10:220. https://doi.org/10.3389/fpls.2019.00220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan GY, Xing YJ, Wang JY, Li ZH, Wang LG, Wang QG, Xu LJ, Zhang Z, Zhang JH, Dong XD, Shan WJ, Guo L, Han SJ (2018) Sequestration of atmospheric CO2 in boreal forest carbon pools in northeastern China: effects of nitrogen deposition. Agric For Meteorol 248:70–81

    Article  Google Scholar 

  • Yip DZ, Veach AM, Yang ZK, Cregger MA, Schadt CW (2019) Methanogenic archaea dominate mature heartwood habitats of Eastern Cottonwood (Populus deltoides). New Phytol 222:115–121

    Article  CAS  Google Scholar 

  • Zeikus J, Henning D (1975) Methanobacterium arbophilicum sp. nov. an obligate anaerobe isolated from wetwood of living trees. Antonie Van Leeuwenhoek J Microbiol 41:543–552

    Article  CAS  Google Scholar 

  • Zeikus JG, Ward JC (1974) Methane formation in living trees: a microbial origin. Science 184:1181–1183

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was jointly funded by the National Key Research and Development Program of China (2016YFA0600803), the National Natural Science Foundation of China (31770501), and China Major Science and Technology Program for Water Pollution Control and Treatment (2017ZX07101003). We thank Dr. Alex Boon of Soil Science Editing for helping to improve the English language.

Author information

Authors and Affiliations

  1. State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences, Nanxincun 20, Xiangshan, Beijing, 100093, China

    Huan-Long Li, Feng-Dan Deng, Xing-Guo Han & Zhi-Ping Wang

  2. University of Chinese Academy of Sciences, Yuquanlu, Beijing, 100049, China

    Huan-Long Li & Xing-Guo Han

  3. Key Laboratory of Dryland Agriculture, MOA, Institute of Environment and Sustainable Development in Agriculture, Chinese Academy of Agricultural Sciences, Beijing, 100081, China

    Xi-Mei Zhang

  4. College of Life and Environmental Sciences, Minzu University of China, Beijing, 100081, China

    Chun-Wang Xiao

  5. School of Life Sciences, Henan University, Kaifeng, 475004, Henan, China

    Shi-Jie Han

Authors
  1. Huan-Long Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xi-Mei Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Feng-Dan Deng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xing-Guo Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chun-Wang Xiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shi-Jie Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zhi-Ping Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Chun-Wang Xiao or Zhi-Ping Wang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by R. Grote.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, HL., Zhang, XM., Deng, FD. et al. Microbial methane production is affected by secondary metabolites in the heartwood of living trees in upland forests. Trees 34, 243–254 (2020). https://doi.org/10.1007/s00468-019-01914-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-019-01914-6

Keywords

Search

Navigation