Global Change Biology Global Change Biology (2014) 20, 2379–2380, doi: 10.1111/gcb.12487
LETTER
Ethylene rather than dissolved organic carbon controls methane uptake in upland soils XIAOQI ZHOU1, HAIBO DONG1, CHENGRONG CHEN1, SIMEON J. SMAILL2 and P E T E R W . C L I N T O N 2 1 Environmental Futures Centre and Griffith School of Environment, Griffith University, Nathan 4111, Australia, 2 Scion, P.O. Box 29237, Fendalton, Christchurch 8540, New Zealand Comments on Sullivan et al. (2013) ‘Does dissolved organic carbon regulate biological methane oxidation in semiarid soils?’ Global Change Biology, 19, 2149-2157.
Sullivan et al. (2013) reported that there was a significantly positive relationship (P < 0.01, r2 = 0.58) between dissolved organic carbon (DOC) using salt extraction methods and potential methane oxidation rates in an arid region across a substrate age gradient. The authors observed that during the wet season rates of methane oxidation were higher, in opposition to trends in other ecosystems where increased soil moisture limits methane oxidation. Furthermore, DOC was more closely correlated with potential methane oxidation rates than other relevant parameters such as soil moisture content, pore space and texture. After considering alternative options, the authors indicated that DOC may be an important regulator of methane oxidation rates in these arid soils. The authors indicated that this conclusion was supported by observations that incubation with 13C-glucose enriched the methaneoxidizing bacteria (MOB) biomarker 18:1x7c, suggesting that DOC was a facultative substrate for MOB, and also explaining the observed correlation. However, as the authors correctly point out, not all organisms containing the 18:1x7c biomarker are MOB, and not all MOB possess this biomarker (Frosteg ard & B a ath, 1996). Therefore, the conclusion that MOB can utilize DOC is not fully convincing as other bacteria may be contributing to the observed results. Furthermore, past research indicates that MOB substrate utilization is highly constrained (Hanson & Hanson, 1996). It is known that MOB can facultatively use methanol, methylamine, and trimethylamine (Hanson & Hanson, 1996), but more specific experimental work is needed to support the assertion that MOB can facultatively use DOC as a carbon and energy source. Here we suggest an alternative explanation for the observed results, based on existing research and recently developed hypotheses relating to the linkages Correspondence: Chengrong Chen, tel. +61 7 37357494, fax +61 7 37357459, e-mail: [email protected]; Simeon J. Smaill, tel. +64 3 3642949 (ext. 7833), fax +64 3 3642812, e-mail: simeon. [email protected]
© 2013 John Wiley & Sons Ltd
between plant stress responses, ethylene production and to methane oxidation in soil (Zhou et al., 2013). When stressed by conditions such as drought, the production of ethylene in most plants is greatly stimulated, increasing ethylene concentrations in the soil atmosphere due to root diffusion (Morgan & Drew, 1997). It has been established that ethylene readily inhibits methane oxidation by competing for the enzyme methane monooxygenase (Kolb, 2009). This effect has been observed at very low concentrations of ethylene, well within the range that can be reached following an event that induces plant stress (J€ackel et al., 2004). We propose that in the wet season the increased availability of moisture promotes a reduction in plant stress, decreasing soil gas ethylene concentrations, and thereby increasing the rate of methane oxidation (cf. Zhou et al., 2013), as observed in Sullivan et al. (2013). This is illustrated conceptually in Fig. 1. This trend could also explain the observed correlation between DOC and methane oxidation, as reductions in plant stress would increase photosynthetic activity, and therefore belowground carbon allocation and DOC inputs to the soil (Br€ uggemann et al., 2011).
Fig. 1 Conceptual model describing how soil moisture availability may affect methane oxidation rates.
2379
2380 X . Z H O U et al. The explanation we propose is supported by some studies of the factors influencing methane oxidation, plant stress and productivity. In situ methane uptake has been positively correlated with aboveground plant biomass in Inner Mongolian semi-arid grasslands (Chen et al., 2011), which is pertinent given the relationship between plant biomass and soil DOC (Br€ uggemann et al., 2011). Research with the enzyme 1aminocyclopropane-1-carboxylate, which regulates in planta ethylene synthesis, has found that reductions in ethylene production can increase plant productivity by attenuating plant stress response (e.g., Belimov et al., 2009). However, there is no reported research that explicitly tests the concept that plant stress can influence methane oxidation rates in soil, or the possibility that DOC can stimulate methane oxidation. We are currently engaged in experimental work to improve understanding of the putative link between plant stress, ethylene production and methane oxidation, and will be in a position to expand this work to include an examination of the effects of DOC on methane oxidation rates in the near future. The results of these experiments will help resolve the uncertainty regarding the mechanisms responsible for the observed phenomena.
Acknowledgements This analysis was jointly supported by a Griffith University Research Fellowship, the Australian Research Council (FT0990547) and a Postdoctoral Research Fellowship at Scion, New Zealand.
References Belimov AA, Dodd IC, Hontzeas N, Theobald JC, Safronova VI, Davies WJ (2009) Rhizosphere bacteria containing 1-aminocyclopropane-1-carboxylate deaminase increase yield of plants grown in drying soil via both local and systemic hormone signalling. New Phytologist, 181, 413–423. Br€ uggemann N, Gessler A, Kayler Z et al. (2011) Carbon allocation and carbon isotope fluxes in the plant-soil-atmosphere continuum: a review. Biogeosciences, 8, 3457–3489. Chen WW, Wolf B, Zheng XH et al. (2011) Annual methane uptake by temperate semiarid steppes as regulated by stocking rates, aboveground plant biomass and topsoil air permeability. Global Change Biology, 17, 2803–2816. Frosteg ard A, B a ath E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biology and Fertility of Soils, 48, 621–631. Hanson R, Hanson T (1996) Methanotrophic bacteria. Microbiology Review, 60, 439–471. J€ackel U, Schnell S, Conrad R (2004) Microbial ethylene production and inhibition of methanotrophic activity in a deciduous forest soil. Soil Biology and Biochemistry, 36, 835–840. Kolb S (2009) The quest for atmospheric methane oxidizers in forest soils. Environmental Microbiology Reports, 1, 336–346. Morgan PW, Drew CD (1997) Ethylene and plant responses to stress. Physiologia Plantarum, 100, 620–630. Sullivan BW, Selmants PC, Hart SC (2013) Does dissolved organic carbon regulate biological methane oxidation in semiarid soils? Global Change Biology, 19, 2149–2157. Zhou X, Smaill SJ, Clinton PW (2013) Methane oxidation needs less stressed plants. Trends in Plant Science, 18, 657–659.
© 2013 John Wiley & Sons Ltd, Global Change Biology, 20, 2379–2380
LETTER
Ethylene rather than dissolved organic carbon controls methane uptake in upland soils XIAOQI ZHOU1, HAIBO DONG1, CHENGRONG CHEN1, SIMEON J. SMAILL2 and P E T E R W . C L I N T O N 2 1 Environmental Futures Centre and Griffith School of Environment, Griffith University, Nathan 4111, Australia, 2 Scion, P.O. Box 29237, Fendalton, Christchurch 8540, New Zealand Comments on Sullivan et al. (2013) ‘Does dissolved organic carbon regulate biological methane oxidation in semiarid soils?’ Global Change Biology, 19, 2149-2157.
Sullivan et al. (2013) reported that there was a significantly positive relationship (P < 0.01, r2 = 0.58) between dissolved organic carbon (DOC) using salt extraction methods and potential methane oxidation rates in an arid region across a substrate age gradient. The authors observed that during the wet season rates of methane oxidation were higher, in opposition to trends in other ecosystems where increased soil moisture limits methane oxidation. Furthermore, DOC was more closely correlated with potential methane oxidation rates than other relevant parameters such as soil moisture content, pore space and texture. After considering alternative options, the authors indicated that DOC may be an important regulator of methane oxidation rates in these arid soils. The authors indicated that this conclusion was supported by observations that incubation with 13C-glucose enriched the methaneoxidizing bacteria (MOB) biomarker 18:1x7c, suggesting that DOC was a facultative substrate for MOB, and also explaining the observed correlation. However, as the authors correctly point out, not all organisms containing the 18:1x7c biomarker are MOB, and not all MOB possess this biomarker (Frosteg ard & B a ath, 1996). Therefore, the conclusion that MOB can utilize DOC is not fully convincing as other bacteria may be contributing to the observed results. Furthermore, past research indicates that MOB substrate utilization is highly constrained (Hanson & Hanson, 1996). It is known that MOB can facultatively use methanol, methylamine, and trimethylamine (Hanson & Hanson, 1996), but more specific experimental work is needed to support the assertion that MOB can facultatively use DOC as a carbon and energy source. Here we suggest an alternative explanation for the observed results, based on existing research and recently developed hypotheses relating to the linkages Correspondence: Chengrong Chen, tel. +61 7 37357494, fax +61 7 37357459, e-mail: [email protected]; Simeon J. Smaill, tel. +64 3 3642949 (ext. 7833), fax +64 3 3642812, e-mail: simeon. [email protected]
© 2013 John Wiley & Sons Ltd
between plant stress responses, ethylene production and to methane oxidation in soil (Zhou et al., 2013). When stressed by conditions such as drought, the production of ethylene in most plants is greatly stimulated, increasing ethylene concentrations in the soil atmosphere due to root diffusion (Morgan & Drew, 1997). It has been established that ethylene readily inhibits methane oxidation by competing for the enzyme methane monooxygenase (Kolb, 2009). This effect has been observed at very low concentrations of ethylene, well within the range that can be reached following an event that induces plant stress (J€ackel et al., 2004). We propose that in the wet season the increased availability of moisture promotes a reduction in plant stress, decreasing soil gas ethylene concentrations, and thereby increasing the rate of methane oxidation (cf. Zhou et al., 2013), as observed in Sullivan et al. (2013). This is illustrated conceptually in Fig. 1. This trend could also explain the observed correlation between DOC and methane oxidation, as reductions in plant stress would increase photosynthetic activity, and therefore belowground carbon allocation and DOC inputs to the soil (Br€ uggemann et al., 2011).
Fig. 1 Conceptual model describing how soil moisture availability may affect methane oxidation rates.
2379
2380 X . Z H O U et al. The explanation we propose is supported by some studies of the factors influencing methane oxidation, plant stress and productivity. In situ methane uptake has been positively correlated with aboveground plant biomass in Inner Mongolian semi-arid grasslands (Chen et al., 2011), which is pertinent given the relationship between plant biomass and soil DOC (Br€ uggemann et al., 2011). Research with the enzyme 1aminocyclopropane-1-carboxylate, which regulates in planta ethylene synthesis, has found that reductions in ethylene production can increase plant productivity by attenuating plant stress response (e.g., Belimov et al., 2009). However, there is no reported research that explicitly tests the concept that plant stress can influence methane oxidation rates in soil, or the possibility that DOC can stimulate methane oxidation. We are currently engaged in experimental work to improve understanding of the putative link between plant stress, ethylene production and methane oxidation, and will be in a position to expand this work to include an examination of the effects of DOC on methane oxidation rates in the near future. The results of these experiments will help resolve the uncertainty regarding the mechanisms responsible for the observed phenomena.
Acknowledgements This analysis was jointly supported by a Griffith University Research Fellowship, the Australian Research Council (FT0990547) and a Postdoctoral Research Fellowship at Scion, New Zealand.
References Belimov AA, Dodd IC, Hontzeas N, Theobald JC, Safronova VI, Davies WJ (2009) Rhizosphere bacteria containing 1-aminocyclopropane-1-carboxylate deaminase increase yield of plants grown in drying soil via both local and systemic hormone signalling. New Phytologist, 181, 413–423. Br€ uggemann N, Gessler A, Kayler Z et al. (2011) Carbon allocation and carbon isotope fluxes in the plant-soil-atmosphere continuum: a review. Biogeosciences, 8, 3457–3489. Chen WW, Wolf B, Zheng XH et al. (2011) Annual methane uptake by temperate semiarid steppes as regulated by stocking rates, aboveground plant biomass and topsoil air permeability. Global Change Biology, 17, 2803–2816. Frosteg ard A, B a ath E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biology and Fertility of Soils, 48, 621–631. Hanson R, Hanson T (1996) Methanotrophic bacteria. Microbiology Review, 60, 439–471. J€ackel U, Schnell S, Conrad R (2004) Microbial ethylene production and inhibition of methanotrophic activity in a deciduous forest soil. Soil Biology and Biochemistry, 36, 835–840. Kolb S (2009) The quest for atmospheric methane oxidizers in forest soils. Environmental Microbiology Reports, 1, 336–346. Morgan PW, Drew CD (1997) Ethylene and plant responses to stress. Physiologia Plantarum, 100, 620–630. Sullivan BW, Selmants PC, Hart SC (2013) Does dissolved organic carbon regulate biological methane oxidation in semiarid soils? Global Change Biology, 19, 2149–2157. Zhou X, Smaill SJ, Clinton PW (2013) Methane oxidation needs less stressed plants. Trends in Plant Science, 18, 657–659.
© 2013 John Wiley & Sons Ltd, Global Change Biology, 20, 2379–2380
