A Meta-analysis of the Effects of Warming and Elevated CO2 on Soil Microbes

doi:10.5814/j.issn.1674-764X.2019.01.009

Abstract

Abstract:

Soil microbes play important roles in terrestrial ecosystem carbon and nitrogen cycling. Climatic warming and elevated CO₂are two aspects of climatic change. In this study, we used a meta-analysis approach to synthesise observations related to the effects of warming and elevated CO₂on soil microbial biomass and community structure. Ecosystem types were mainly grouped into forests and grasslands. Warming methods included open top chambers and infrared radiators. Experimental settings included all-day warming, daytime warming and nighttime warming. Warming increased soil actinomycetes and saprotrophic fungi, while elevated CO₂ decreased soil gram-positive bacteria (G⁺). Mean annual temperature and mean annual precipitation were negatively correlated with warming effects on gram-negative bacteria (G^-) and total phospholipid fatty acid (PLFA), respectively. Elevation was positively correlated with the warming effect on total PLFA, bacteria, G⁺and G^-. Grassland exhibited a positive response of total PLFA and actinomycetes to warming, while forest exhibited a positive response in the ratio of soil fungi to bacteria (F/B ratio) to warming. The open top chamber method increased G^-, while the infrared radiator method decreased the F/B ratio. Daytime warming rather than all-day warming increased G^-. Our findings indicated that the effects of warming on soil microbes differed with ecosystem types, warming methods, warming times, elevation and local climate conditions.

Key words: ecosystem types, elevated CO₂, increased temperature, response ratio, warming methods

FU Gang,ZHANG Haorui,LI Shaowei,SUN Wei. A Meta-analysis of the Effects of Warming and Elevated CO₂ on Soil Microbes[J]. Journal of Resources and Ecology, 2019, 10(1): 69-76.

Figures/Tables 7

References 40

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Authors	Year	Journal	Title	MAT (℃)	MAP (mm)	Elevation (m)	Latitude	Longitude	Vegetation types
Wang et al.	2011	Chinese Journal of Applied and Environmental Biology	Microbial communities of alpine meadow soil in the Eastern Qinghai-Tibetan Plateau subjected to experimental warming and grazing	1.1	752.4	3561	32.45	102.37	Grassland
Schindlbacher et al.	2011	Soil Biology & Biochemistry	Experimental warming effects on the microbial community of a temperate mountain forest soil	5.7	1480	910	47.58	11.64	Forest
Andresen et al.	2014	PLoS ONE	Bacteria and fungi respond differently to multifactorial climate change in a temperate heathland, traced with 13C-glycine and FACE CO₂	8	600		55.88	11.97	Tundra
Rinnan et al.	2007	Global Change Biology	Fifteen years of climate change manipulations alter soil microbial communities in a subarctic heath ecosystem	-0.4	245.5	450	68.35	18.82	Tundra
Rousk et al.	2013	Global Change Biology	Investigating the long-term legacy of drought and warming on the soil microbial community across five European shrubland ecosystems				56.38	10.95	Shrubland
							46.88	19.72	Shrubland
							40.60	8.15	Shrubland
							52.40	5.92	Shrubland
							53.05	-3.47	Shrubland
Zhou et al.	2012	Nature Climate Change	Microbial mediation of carbon-cycle feedbacks to climate warming	16.3	914		34.98	-97.52	Grassland
Zhao et al.	2014	Plant and Soil	Effects of experimental warming and nitrogen fertilization on soil microbial communities and processes of two subalpine coniferous species in Eastern Tibetan Plateau, China	8.9	919.5	1820	31.68	103.88	Forest
Zhang et al.	2014	PLoS ONE	Responses of soil microbial communities to experimental warming in alpine grasslands on the Qinghai-Tibet Plateau	-3.8	290.9	4635	34.82	92.93	Grassland
Zhang et al.	2011	Soil Biology & Biochemistry	Soil microbial community changes and their linkages with ecosystem carbon exchange under asymmetrically diurnal warming	2.1	383	1324	42.03	116.28	Grassland
Shen et al.	2014	Pedosphere	Soil microbial responses to experimental warming and nitrogen addition in a temperate steppe of Northern China	2.1	383	1324	42.03	116.28	Grassland
Zhang et al.	2013	Oecologia	Soil microbial responses to warming and increased precipitation and their implications for ecosystem C cycling	2.1	383	1324	42.03	116.28	Grassland
Wang et al.	2014	Acta Ecologica Sinica	Effects of warming on soil microbial community structure in Changbai Mountain tundra	-7.3	1600	2028			Tundra
Gutknecht et al.	2012	Global Change Biology	Microbial communities and their responses to simulated global change fluctuate greatly over multiple years				37.67	-122.37	Grassland
Xu et al.	2015	Soil Biology & Biochemistry	Labile, recalcitrant, microbial carbon and nitrogen and the microbial community composition at two Abies faxoniana forest elevations under elevated temperatures	2.7	813	3000			Forest
Maestre et al.	2015	Frontiers in Microbiology	Warming reduces the cover and diversity of biocrust-forming mosses and lichens, and increases the physiological stress of soil microbial communities in a semi-arid Pinus halepensis plantation	14.6	315		38.54	-49.00	Forest
Zhang et al.	2015	European Journal of Soil Science	Depth-related responses of soil microbial communities to experimental warming in an alpine meadow on the Qinghai-Tibet Plateau	-3.8	383	4635	34.85	92.93	Grassland
De Long et al.	2016	Ecosystems	Contrasting responses of soil microbial and nematode communities to warming and plant functional group removal across a post-fire boreal forest successional gradient						Forest
Yoshitake et al.	2015	Ecological Research	Soil microbial response to experimental warming in cool temperate semi-natural grassland in Japan	7.1	2128		36.13	137.42	Grassland
Authors	Year	Journal	Title	MAT (℃)	MAP (mm)	Elevation (m)	Latitude	Longitude	Vegetation types
Kao-Kniffin et al.	2013	Microbial Ecology	A microbial link between elevated CO₂ and methane emissions that is plant species-specific						Grassland
Feng et al.	2010	Global Change Biology	Altered microbial community structure and organic matter composition under elevated CO₂ and N fertilization in the duke forest				35.97	-79.08	Forest
Kasurinen et al.	2005	Global Change Biology	Below-ground responses of silver birch trees exposed to elevated CO₂ and O₃ levels during three growing seasons		307.33	120	62.65	27.05	Forest
Kanerva et al.	2008	Soil Biology & Biochemistry	Changes in soil microbial community structure under elevated changes in soil microbial community structure under elevated tropospheric O₃ and CO₂				60.82	23.47	Grassland
Ebersberger et al.	2004	Plant and Soil	Effects of long term CO₂ enrichment on microbial community structure in calcareous grassland	8.75	900	520	47.55	7.57	Grassland
Janus et al.	2005	Microbial Ecology	Elevated atmospheric CO₂alters soil microbial communities associated with trembling aspen (Populus tremuloides) roots				45.57	-84.67	Forest
Hagedorn et al.	2013	Soil Biology & Biochemistry	Nine years of CO₂ enrichment at the alpine treeline stimulates soil respiration but does not alter soil microbial communities				47.47	7.50	Forest
Manninen et al.	2010	Soil Biology & Biochemistry	Plant and soil microbial biomasses in Agrostis capillaris and Lathyrus pratensis monocultures exposed to elevated O₃ and CO₂ for three growing seasons				60.82	23.47	Grassland
Chung et al.	2007	Global Change Biology	Plant species richness, elevated CO₂, and atmospheric nitrogen deposition alter soil microbial community composition and function						Grassland
Guenet et al.	2012	Geoderma	The impact of long-term CO₂ enrichment and moisture levels on soil microbial community structure and enzyme activities						Grassland

Authors	Year	Journal	Title	MAT (℃)	MAP (mm)	Elevation (m)	Latitude	Longitude	Vegetation types
Wang et al.	2011	Chinese Journal of Applied and Environmental Biology	Microbial communities of alpine meadow soil in the Eastern Qinghai-Tibetan Plateau subjected to experimental warming and grazing	1.1	752.4	3561	32.45	102.37	Grassland
Schindlbacher et al.	2011	Soil Biology & Biochemistry	Experimental warming effects on the microbial community of a temperate mountain forest soil	5.7	1480	910	47.58	11.64	Forest
Andresen et al.	2014	PLoS ONE	Bacteria and fungi respond differently to multifactorial climate change in a temperate heathland, traced with 13C-glycine and FACE CO₂	8	600		55.88	11.97	Tundra
Rinnan et al.	2007	Global Change Biology	Fifteen years of climate change manipulations alter soil microbial communities in a subarctic heath ecosystem	-0.4	245.5	450	68.35	18.82	Tundra
Rousk et al.	2013	Global Change Biology	Investigating the long-term legacy of drought and warming on the soil microbial community across five European shrubland ecosystems				56.38	10.95	Shrubland
							46.88	19.72	Shrubland
							40.60	8.15	Shrubland
							52.40	5.92	Shrubland
							53.05	-3.47	Shrubland
Zhou et al.	2012	Nature Climate Change	Microbial mediation of carbon-cycle feedbacks to climate warming	16.3	914		34.98	-97.52	Grassland
Zhao et al.	2014	Plant and Soil	Effects of experimental warming and nitrogen fertilization on soil microbial communities and processes of two subalpine coniferous species in Eastern Tibetan Plateau, China	8.9	919.5	1820	31.68	103.88	Forest
Zhang et al.	2014	PLoS ONE	Responses of soil microbial communities to experimental warming in alpine grasslands on the Qinghai-Tibet Plateau	-3.8	290.9	4635	34.82	92.93	Grassland
Zhang et al.	2011	Soil Biology & Biochemistry	Soil microbial community changes and their linkages with ecosystem carbon exchange under asymmetrically diurnal warming	2.1	383	1324	42.03	116.28	Grassland
Shen et al.	2014	Pedosphere	Soil microbial responses to experimental warming and nitrogen addition in a temperate steppe of Northern China	2.1	383	1324	42.03	116.28	Grassland
Zhang et al.	2013	Oecologia	Soil microbial responses to warming and increased precipitation and their implications for ecosystem C cycling	2.1	383	1324	42.03	116.28	Grassland
Wang et al.	2014	Acta Ecologica Sinica	Effects of warming on soil microbial community structure in Changbai Mountain tundra	-7.3	1600	2028			Tundra
Gutknecht et al.	2012	Global Change Biology	Microbial communities and their responses to simulated global change fluctuate greatly over multiple years				37.67	-122.37	Grassland
Xu et al.	2015	Soil Biology & Biochemistry	Labile, recalcitrant, microbial carbon and nitrogen and the microbial community composition at two Abies faxoniana forest elevations under elevated temperatures	2.7	813	3000			Forest
Maestre et al.	2015	Frontiers in Microbiology	Warming reduces the cover and diversity of biocrust-forming mosses and lichens, and increases the physiological stress of soil microbial communities in a semi-arid Pinus halepensis plantation	14.6	315		38.54	-49.00	Forest
Zhang et al.	2015	European Journal of Soil Science	Depth-related responses of soil microbial communities to experimental warming in an alpine meadow on the Qinghai-Tibet Plateau	-3.8	383	4635	34.85	92.93	Grassland
De Long et al.	2016	Ecosystems	Contrasting responses of soil microbial and nematode communities to warming and plant functional group removal across a post-fire boreal forest successional gradient						Forest
Yoshitake et al.	2015	Ecological Research	Soil microbial response to experimental warming in cool temperate semi-natural grassland in Japan	7.1	2128		36.13	137.42	Grassland
Authors	Year	Journal	Title	MAT (℃)	MAP (mm)	Elevation (m)	Latitude	Longitude	Vegetation types
Kao-Kniffin et al.	2013	Microbial Ecology	A microbial link between elevated CO₂ and methane emissions that is plant species-specific						Grassland
Feng et al.	2010	Global Change Biology	Altered microbial community structure and organic matter composition under elevated CO₂ and N fertilization in the duke forest				35.97	-79.08	Forest
Kasurinen et al.	2005	Global Change Biology	Below-ground responses of silver birch trees exposed to elevated CO₂ and O₃ levels during three growing seasons		307.33	120	62.65	27.05	Forest
Kanerva et al.	2008	Soil Biology & Biochemistry	Changes in soil microbial community structure under elevated changes in soil microbial community structure under elevated tropospheric O₃ and CO₂				60.82	23.47	Grassland
Ebersberger et al.	2004	Plant and Soil	Effects of long term CO₂ enrichment on microbial community structure in calcareous grassland	8.75	900	520	47.55	7.57	Grassland
Janus et al.	2005	Microbial Ecology	Elevated atmospheric CO₂alters soil microbial communities associated with trembling aspen (Populus tremuloides) roots				45.57	-84.67	Forest
Hagedorn et al.	2013	Soil Biology & Biochemistry	Nine years of CO₂ enrichment at the alpine treeline stimulates soil respiration but does not alter soil microbial communities				47.47	7.50	Forest
Manninen et al.	2010	Soil Biology & Biochemistry	Plant and soil microbial biomasses in Agrostis capillaris and Lathyrus pratensis monocultures exposed to elevated O₃ and CO₂ for three growing seasons				60.82	23.47	Grassland
Chung et al.	2007	Global Change Biology	Plant species richness, elevated CO₂, and atmospheric nitrogen deposition alter soil microbial community composition and function						Grassland
Guenet et al.	2012	Geoderma	The impact of long-term CO₂ enrichment and moisture levels on soil microbial community structure and enzyme activities						Grassland

Variables	Slope	p	Q_M	Q_E	Q_T	n
Warming duration
Total PLFA	-0.01	0.633	0.23	29.21	29.44	28
Fungi	0.01	0.568	0.33	24.81	25.13	28
Bacteria	0.01	0.394	0.73	29.67	30.39	29
G⁺	0.03	0.417	0.66	20.04	20.69	20
G^-	0.01	0.849	0.04	18.21	18.25	18
F/B ratio	-0.01	0.471	0.52	18.79	19.31	22
Warming magnitude
Total PLFA	-0.02	0.819	0.05	27.44	27.49	24
Fungi	0.05	0.517	0.42	22.01	22.43	26
Bacteria	0.01	0.887	0.02	27.36	27.38	26
G⁺	0.01	0.904	0.01	22.38	22.39	21
G^-	0.03	0.580	0.31	19.21	19.52	19
F/B ratio	-0.01	0.815	0.05	16.16	16.21	19
Mean annual air temperature
Total PLFA	-0.01	0.451	0.57	18.44	19.00	20
Fungi	-0.01	0.366	0.82	14.80	15.62	20
Bacteria	-0.01	0.269	1.22	17.68	18.90	21
G⁺	-0.01	0.166	1.92	22.23	24.16	20
G^-	-0.02	0.014	6.09	19.75	25.84	18
F/B ratio	-0.0021	0.633	0.23	16.55	16.78	19
Mean annual precipitation
Total PLFA	-0.0002	0.019	5.54	24.16	29.70	19
Fungi	-0.0002	0.077	5.15	19.67	24.82	19
Bacteria	-0.0001	0.244	1.36	19.22	20.58	20
G⁺	-0.0002	0.109	2.57	19.34	21.91	20
G^-	-0.0002	0.208	1.58	18.43	20.01	18
F/B ratio	0.0000	0.597	0.28	14.33	14.61	18
Elevation
Total PLFA	0.0001	0.031	4.63	16.81	21.45	17
Fungi	0.00	0.366	0.82	15.94	16.76	17
Bacteria	0.0001	0.018	5.63	15.45	21.09	17
G⁺	0.0001	0.010	6.63	19.30	25.93	17
G^-	0.0001	0.034	4.51	19.65	24.16	16

Variables	Slope	p	Q_M	Q_E	Q_T	n
Warming duration
Total PLFA	-0.01	0.633	0.23	29.21	29.44	28
Fungi	0.01	0.568	0.33	24.81	25.13	28
Bacteria	0.01	0.394	0.73	29.67	30.39	29
G⁺	0.03	0.417	0.66	20.04	20.69	20
G^-	0.01	0.849	0.04	18.21	18.25	18
F/B ratio	-0.01	0.471	0.52	18.79	19.31	22
Warming magnitude
Total PLFA	-0.02	0.819	0.05	27.44	27.49	24
Fungi	0.05	0.517	0.42	22.01	22.43	26
Bacteria	0.01	0.887	0.02	27.36	27.38	26
G⁺	0.01	0.904	0.01	22.38	22.39	21
G^-	0.03	0.580	0.31	19.21	19.52	19
F/B ratio	-0.01	0.815	0.05	16.16	16.21	19
Mean annual air temperature
Total PLFA	-0.01	0.451	0.57	18.44	19.00	20
Fungi	-0.01	0.366	0.82	14.80	15.62	20
Bacteria	-0.01	0.269	1.22	17.68	18.90	21
G⁺	-0.01	0.166	1.92	22.23	24.16	20
G^-	-0.02	0.014	6.09	19.75	25.84	18
F/B ratio	-0.0021	0.633	0.23	16.55	16.78	19
Mean annual precipitation
Total PLFA	-0.0002	0.019	5.54	24.16	29.70	19
Fungi	-0.0002	0.077	5.15	19.67	24.82	19
Bacteria	-0.0001	0.244	1.36	19.22	20.58	20
G⁺	-0.0002	0.109	2.57	19.34	21.91	20
G^-	-0.0002	0.208	1.58	18.43	20.01	18
F/B ratio	0.0000	0.597	0.28	14.33	14.61	18
Elevation
Total PLFA	0.0001	0.031	4.63	16.81	21.45	17
Fungi	0.00	0.366	0.82	15.94	16.76	17
Bacteria	0.0001	0.018	5.63	15.45	21.09	17
G⁺	0.0001	0.010	6.63	19.30	25.93	17
G^-	0.0001	0.034	4.51	19.65	24.16	16

A Meta-analysis of the Effects of Warming and Elevated CO₂ on Soil Microbes

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