青藏高原高寒草地土壤微生物群落及影响因子
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摘要
青藏高原是我国生态安全的重要屏障,但目前青藏高原上大尺度上的微生物地理学研究还很缺乏.因此,采用高通量测序技术,在跨越2121 km的尺度上针对高寒草地不同生态系统类型研究了土壤原核生物(细菌和古菌)微生物量、多样性和群落组成的分布格局,及与气候、植物和土壤因子的关系.在高寒草甸、高寒草原、高寒灌丛和高寒荒漠中,高寒荒漠具有最低的微生物多样性,而高寒草甸具有最高的微生物量碳.高寒草地土壤微生物的多样性与大气温度而非降水显著相关,说明其在高寒条件下可能受温度而非水分控制.微生物多样性随耦合了水、热要素的干旱指数的增加而降低,解释量比单一要素更高.此外,植物功能群多样性与微生物多样性有显著的正相关关系,解释量比植物物种多样性更高.结构方程模型显示,干旱指数和年均温通过影响植物功能群多样性和地上生物量而改变土壤表层的碳氮比,从而直接或间接影响到微生物多样性.与多样性不同,土壤微生物量碳与可溶性有机碳、氨态氮、速效磷及碳氮比等土壤营养指标和植物地上生物量具有显著的相关性.这些结果意味着微生物多样性和微生物量可能有着不同的控制因子;随着未来青藏高原的"暖湿化",干旱指数的降低可能提高土壤微生物的多样性.
As an indicator and regulator of climate and environmental change, the Tibetan Plateau is an important barrier for ecological security. However, despite the importance of soil microbial communities in almost all soil biochemical processes and ecosystem functions, the biogeography of soil microbial communities on the Tibetan Plateau is poorly understood, especially at large scales over different ecosystem types. In this study, we collected samples from 64 sampling sites representing different grassland ecosystem types and spanning 2121 km across on the Tibetan Plateau. We then used next generation high-throughput sequencing to investigate the soil prokaryote community(i.e. bacteria and archaea) diversity and spatial patterns and to explore their relationship with biotic(e.g. plant functional group diversity and biomass) and abiotic(e.g. aridity index, soil carbon and nitrogen levels) factors. Among the four alpine grassland types(i.e. alpine meadow, alpine steppe, alpine shrub and alpine desert) sampled in this study, alpine meadow had the highest soil microbial biomass and alpine desert had the lowest soil microbial richness and Shannon diversity. The soil microbial diversity in the alpine grassland correlated with plant diversity and climate factors. Soil microbial diversity negatively correlated with the annual average air temperature, but was not correlated with the annual average precipitation, indicating that temperature, rather than precipitation, may be more important in controlling the soil microbial diversity in alpine grassland ecosystems at cold temperatures. Higher air temperature likely led to an intensified aridity under limited precipitation, and thus decreased microbial diversity. As a result, the aridity index combined with temperature and precipitation explained more of the variance in the soil microbial diversity than air temperature or precipitation did individually.Moreover, after separating plant species into four functional groups(grass, forb, legume and sedge), microbial diversity positively correlated with plant functional group diversity, explaining more of the variance in microbial diversity than plant species diversity did. Results of structural equation modeling revealed that the aridity index and annual air temperature affected soil microbial diversity, directly or indirectly, through influencing plant functional group diversity and aboveground biomass; while aboveground biomass changed the soil carbon to nitrogen ratio in the upper soil layers and thus impacted soil microbial diversity.However, in contrast to microbial diversity, soil microbial biomass carbon was not correlated with plant functional group diversity,plant species diversity, or the climate factors annual average air temperature, annual precipitation and aridity index, but were linked to soil nutrient status(e.g. soil dissolved organic carbon, ammonia, available phosphorus, and carbon to nitrogen ratio) and plant biomass of sedges and forbs, demonstrating that microbial biomass and diversity were likely controlled by different factors.In summary, this study investigated the spatial patterns of soil microbial communities across different alpine grassland ecosystem types on the Tibetan Plateau and enhanced our understanding of biotic and abiotic factors controlling microbial biomass and diversity, which will be important in predicting microbial changes on the Tibetan Plateau under future climate change. Under future warming and wetting scenarios on the Tibetan Plateau, it is possible that the aridity index would decrease, leading to increased soil microbial diversity. Results of this study also suggest a focus on the aridity index and plant functional group diversity in future microbial biogeography studies in order to further determine their roles in controlling or mediating soil microbial biomass and diversity.
As an indicator and regulator of climate and environmental change, the Tibetan Plateau is an important barrier for ecological security. However, despite the importance of soil microbial communities in almost all soil biochemical processes and ecosystem functions, the biogeography of soil microbial communities on the Tibetan Plateau is poorly understood, especially at large scales over different ecosystem types. In this study, we collected samples from 64 sampling sites representing different grassland ecosystem types and spanning 2121 km across on the Tibetan Plateau. We then used next generation high-throughput sequencing to investigate the soil prokaryote community(i.e. bacteria and archaea) diversity and spatial patterns and to explore their relationship with biotic(e.g. plant functional group diversity and biomass) and abiotic(e.g. aridity index, soil carbon and nitrogen levels) factors. Among the four alpine grassland types(i.e. alpine meadow, alpine steppe, alpine shrub and alpine desert) sampled in this study, alpine meadow had the highest soil microbial biomass and alpine desert had the lowest soil microbial richness and Shannon diversity. The soil microbial diversity in the alpine grassland correlated with plant diversity and climate factors. Soil microbial diversity negatively correlated with the annual average air temperature, but was not correlated with the annual average precipitation, indicating that temperature, rather than precipitation, may be more important in controlling the soil microbial diversity in alpine grassland ecosystems at cold temperatures. Higher air temperature likely led to an intensified aridity under limited precipitation, and thus decreased microbial diversity. As a result, the aridity index combined with temperature and precipitation explained more of the variance in the soil microbial diversity than air temperature or precipitation did individually.Moreover, after separating plant species into four functional groups(grass, forb, legume and sedge), microbial diversity positively correlated with plant functional group diversity, explaining more of the variance in microbial diversity than plant species diversity did. Results of structural equation modeling revealed that the aridity index and annual air temperature affected soil microbial diversity, directly or indirectly, through influencing plant functional group diversity and aboveground biomass; while aboveground biomass changed the soil carbon to nitrogen ratio in the upper soil layers and thus impacted soil microbial diversity.However, in contrast to microbial diversity, soil microbial biomass carbon was not correlated with plant functional group diversity,plant species diversity, or the climate factors annual average air temperature, annual precipitation and aridity index, but were linked to soil nutrient status(e.g. soil dissolved organic carbon, ammonia, available phosphorus, and carbon to nitrogen ratio) and plant biomass of sedges and forbs, demonstrating that microbial biomass and diversity were likely controlled by different factors.In summary, this study investigated the spatial patterns of soil microbial communities across different alpine grassland ecosystem types on the Tibetan Plateau and enhanced our understanding of biotic and abiotic factors controlling microbial biomass and diversity, which will be important in predicting microbial changes on the Tibetan Plateau under future climate change. Under future warming and wetting scenarios on the Tibetan Plateau, it is possible that the aridity index would decrease, leading to increased soil microbial diversity. Results of this study also suggest a focus on the aridity index and plant functional group diversity in future microbial biogeography studies in order to further determine their roles in controlling or mediating soil microbial biomass and diversity.
引文
1 Glassman S I,Weihe C,Li J,et al.Decomposition responses to climate depend on microbial community composition.Proc Natl Acad Sci USA,2018,115:11994-11999
2 Bhatnagar J M,Peay K G,Treseder K K.Litter chemistry influences decomposition through activity of specific microbial functional guilds.Ecol Monogr,2018,88:429-444
3 de Bruijn F J.Biological Nitrogen Fixation,in Principles of Plant-Microbe Interactions:Microbes for Sustainable Agriculture.Cham:Springer International Publishing,2015.215-224
4 Vitousek P M,Cassman K,Cleveland C,et al.Towards an ecological understanding of biological nitrogen fixation.Biogeochemistry,2002,57:1-45
5 Leininger S,Urich T,Schloter M,et al.Archaea predominate among ammonia-oxidizing prokaryotes in soils.Nature,2006,442:806-809
6 Francis C A,Beman J M,Kuypers M M M.New processes and players in the nitrogen cycle:The microbial ecology of anaerobic and archaeal ammonia oxidation.ISME J,2007,1:19-27
7 García-Parisi P A,Omacini M.Arbuscular mycorrhizal fungi can shift plant-soil feedback of grass-endophyte symbiosis from negative to positive.Plant Soil,2017,419:13-23
8 Ke P J,Miki T,Ding T S.The soil microbial community predicts the importance of plant traits in plant-soil feedback.New Phytol,2015,206:329-341
9 Chu H Y,Wang Y F,Shi Y,et al.Current status and development trend of soil microbial biogeography(in Chinese).Bull Chin Acad Sci,2017,32:585-592[褚海燕,王艳芬,时玉,等.土壤微生物生物地理学研究现状与发展态势.中国科学院院刊,2017,32:585-592]
10 Sanders N J,Rahbek C.The patterns and causes of elevational diversity gradients.Ecography,2012,35:1-3
11 Adler P B,Seabloom E W,Borer E T,et al.Productivity is a poor predictor of plant species richness.Science,2011,333:1750-1753
12 O’Brien S L,Gibbons S M,Owens S M,et al.Spatial scale drives patterns in soil bacterial diversity.Environ Microbiol,2016,18:2039-2051
13 Martiny J B H,Bohannan B J M,Brown J H,et al.Microbial biogeography:Putting microorganisms on the map.Nat Rev Microbiol,2006,4:102-112
14 Franklin R B,Mills A L.Importance of spatially structured environmental heterogeneity in controlling microbial community composition at small spatial scales in an agricultural field.Soil Biol Biochem,2009,41:1833-1840
15 Griffiths R I,Thomson B C,James P,et al.The bacterial biogeography of British soils.Environ Microbiol,2011,13:1642-1654
16 Garcia-Pichel F,Loza V,Marusenko Y,et al.Temperature drives the continental-scale distribution of key microbes in topsoil communities.Science,2013,340:1574-1577
17 Curd E E,Martiny J B H,Li H,et al.Bacterial diversity is positively correlated with soil heterogeneity.Ecosphere,2018,9:e02079
18 Juyal A,Otten W,Falconer R,et al.Combination of techniques to quantify the distribution of bacteria in their soil microhabitats at different spatial scales.Geoderma,2019,334:165-174
19 Nemergut D R,Schmidt S K,Fukami T,et al.Patterns and processes of microbial community assembly.Microbiol Mol Biol Rev,2013,77:342-356
20 Fierer N,Jackson R B.The diversity and biogeography of soil bacterial communities.Proc Natl Acad Sci USA,2006,103:626-631
21 Bahram M,Hildebrand F,Forslund S K,et al.Structure and function of the global topsoil microbiome.Nature,2018,560:233-237
22 Maestre F T,Delgado-Baquerizo M,Jeffries T C,et al.Increasing aridity reduces soil microbial diversity and abundance in global drylands.Proc Natl Acad Sci USA,2015,112:15684-15689
23 Zhou J,Deng Y,Shen L,et al.Temperature mediates continental-scale diversity of microbes in forest soils.Nat Commun,2016,7:12083
24 Yao T,Thompson L G,Mosbrugger V,et al.Third pole environment(TPE).Environ Dev,2012,3:52-64
25 Sun H L,Zheng D,Yao T D,et al.Protection and construction of the national ecological security shelter zone on Tibetan Plateau(in Chinese).Acta Geogr Sin,2012,67:3-12[孙鸿烈,郑度,姚檀栋,等.青藏高原国家生态安全屏障保护与建设.地理学报,2012,67:3-12]
26 Chu H,Sun H,Tripathi B M,et al.Bacterial community dissimilarity between the surface and subsurface soils equals horizontal differences over several kilometers in the western Tibetan Plateau.Environ Microbiol,2016,18:1523-1533
27 Duckworth J,Jager T,Ashauer R.Automated,high-throughput measurement of size and growth curves of small organisms in well plates.Sci Rep,2019,9:10
28 Yang T,Adams J M,Shi Y,et al.Soil fungal diversity in natural grasslands of the Tibetan Plateau:Associations with plant diversity and productivity.New Phytol,2017,215:756-765
29 Che R,Deng Y,Wang F,et al.Autotrophic and symbiotic diazotrophs dominate nitrogen-fixing communities in Tibet grassland soils.Sci Total Environ,2018,639:997-1006
30 Zhang J,Wang F,Che R,et al.Precipitation shapes communities of arbuscular mycorrhizal fungi in Tibet alpine steppe.Sci Rep,2016,6:23488
31 Hijmans R J,Cameron S E,Parra J L,et al.Very high resolution interpolated climate surfaces for global land areas.Int J Climatol,2005,25:1965-1978
32 Delgado-Baquerizo M,Maestre F T,Reich P B,et al.Carbon content and climate variability drive global soil bacterial diversity patterns.Ecol Monogr,2016,86:373-390
33 Li Y,Lin Q,Wang S,et al.Soil bacterial community responses to warming and grazing in a Tibet alpine meadow.FEMS Microbiol Ecol,2016:fiv152
34 Spehn E M,Joshi J,Schmid B,et al.Plant diversity effects on soil heterotrophic activity in experimental grassland ecosystems.Plant Soil,2000,224:217-230
35 Weidner S,Koller R,Latz E,et al.Bacterial diversity amplifies nutrient-based plant-soil feedbacks.Funct Ecol,2015,29:1341-1349
36 Prober S M,Leff J W,Bates S T,et al.Plant diversity predicts beta but not alpha diversity of soil microbes across grasslands worldwide.Ecol Lett,2015,18:85-95
37 Lange M,Habekost M,Eisenhauer N,et al.Biotic and abiotic properties mediating plant diversity effects on soil microbial communities in an experimental grassland.PLo S One,2014,9:e96182
38 Hooper D U,Bignell D E,Brown V K,et al.Interactions between aboveground and belowground biodiversity in terrestrial ecosystems:Patterns,mechanisms,and feedbacks.Bio Science,2000,50:1049-1061
39 Wardle D A.The influence of biotic interactions on soil biodiversity.Ecol Lett,2006,9:870-886
40 Millard P,Singh B K.Does grassland vegetation drive soil microbial diversity?Nutr Cycl Agroecosyst,2010,88:147-158
41 Eisenhauer N,Milcu A,Sabais A C W,et al.Plant diversity surpasses plant functional groups and plant productivity as driver of soil biota in the long term.PLo S One,2011,6:e16055
42 Woodward F I,Cramer W.Plant functional types and climatic change:Introduction.J Veg Sci,1996,7:306-308
43 Bonet A.Secondary succession of semi-arid Mediterranean old-fields in south-eastern Spain:Insights for conservation and restoration of degraded lands.J Arid Environ,2004,56:213-233
44 Pausas J G,Austin M P.Patterns of plant species richness in relation to different environments:An appraisal.J Veg Sci,2001,12:153-166
45 Mayfield M M,Levine J M.Opposing effects of competitive exclusion on the phylogenetic structure of communities.Ecol Lett,2010,13:1085-1093
46 Rosindell J,Hubbell S P,He F,et al.The case for ecological neutral theory.Trends Ecol Evol,2012,27:203-208
47 Dini-Andreote F,Stegen J C,van Elsas J D,et al.Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession.Proc Natl Acad Sci USA,2015,112:E1326-E1332
48 Zhou J,Ning D.Stochastic community assembly:Does it matter in microbial ecology?Microbiol Mol Biol Rev,2017,81:e00002
49 Kang S,Xu Y,You Q,et al.Review of climate and cryospheric change in the Tibetan Plateau.Environ Res Lett,2010,5:015101
50 Xu Z X,Gong T L,Li J Y.Decadal trend of climate in the Tibetan Plateau-Regional temperature and precipitation.Hydrol Process,2008,22:3056-3065
51 Kuang X,Jiao J J.Review on climate change on the Tibetan Plateau during the last half century.J Geophys Res Atmos,2016,121:3979-4007
2 Bhatnagar J M,Peay K G,Treseder K K.Litter chemistry influences decomposition through activity of specific microbial functional guilds.Ecol Monogr,2018,88:429-444
3 de Bruijn F J.Biological Nitrogen Fixation,in Principles of Plant-Microbe Interactions:Microbes for Sustainable Agriculture.Cham:Springer International Publishing,2015.215-224
4 Vitousek P M,Cassman K,Cleveland C,et al.Towards an ecological understanding of biological nitrogen fixation.Biogeochemistry,2002,57:1-45
5 Leininger S,Urich T,Schloter M,et al.Archaea predominate among ammonia-oxidizing prokaryotes in soils.Nature,2006,442:806-809
6 Francis C A,Beman J M,Kuypers M M M.New processes and players in the nitrogen cycle:The microbial ecology of anaerobic and archaeal ammonia oxidation.ISME J,2007,1:19-27
7 García-Parisi P A,Omacini M.Arbuscular mycorrhizal fungi can shift plant-soil feedback of grass-endophyte symbiosis from negative to positive.Plant Soil,2017,419:13-23
8 Ke P J,Miki T,Ding T S.The soil microbial community predicts the importance of plant traits in plant-soil feedback.New Phytol,2015,206:329-341
9 Chu H Y,Wang Y F,Shi Y,et al.Current status and development trend of soil microbial biogeography(in Chinese).Bull Chin Acad Sci,2017,32:585-592[褚海燕,王艳芬,时玉,等.土壤微生物生物地理学研究现状与发展态势.中国科学院院刊,2017,32:585-592]
10 Sanders N J,Rahbek C.The patterns and causes of elevational diversity gradients.Ecography,2012,35:1-3
11 Adler P B,Seabloom E W,Borer E T,et al.Productivity is a poor predictor of plant species richness.Science,2011,333:1750-1753
12 O’Brien S L,Gibbons S M,Owens S M,et al.Spatial scale drives patterns in soil bacterial diversity.Environ Microbiol,2016,18:2039-2051
13 Martiny J B H,Bohannan B J M,Brown J H,et al.Microbial biogeography:Putting microorganisms on the map.Nat Rev Microbiol,2006,4:102-112
14 Franklin R B,Mills A L.Importance of spatially structured environmental heterogeneity in controlling microbial community composition at small spatial scales in an agricultural field.Soil Biol Biochem,2009,41:1833-1840
15 Griffiths R I,Thomson B C,James P,et al.The bacterial biogeography of British soils.Environ Microbiol,2011,13:1642-1654
16 Garcia-Pichel F,Loza V,Marusenko Y,et al.Temperature drives the continental-scale distribution of key microbes in topsoil communities.Science,2013,340:1574-1577
17 Curd E E,Martiny J B H,Li H,et al.Bacterial diversity is positively correlated with soil heterogeneity.Ecosphere,2018,9:e02079
18 Juyal A,Otten W,Falconer R,et al.Combination of techniques to quantify the distribution of bacteria in their soil microhabitats at different spatial scales.Geoderma,2019,334:165-174
19 Nemergut D R,Schmidt S K,Fukami T,et al.Patterns and processes of microbial community assembly.Microbiol Mol Biol Rev,2013,77:342-356
20 Fierer N,Jackson R B.The diversity and biogeography of soil bacterial communities.Proc Natl Acad Sci USA,2006,103:626-631
21 Bahram M,Hildebrand F,Forslund S K,et al.Structure and function of the global topsoil microbiome.Nature,2018,560:233-237
22 Maestre F T,Delgado-Baquerizo M,Jeffries T C,et al.Increasing aridity reduces soil microbial diversity and abundance in global drylands.Proc Natl Acad Sci USA,2015,112:15684-15689
23 Zhou J,Deng Y,Shen L,et al.Temperature mediates continental-scale diversity of microbes in forest soils.Nat Commun,2016,7:12083
24 Yao T,Thompson L G,Mosbrugger V,et al.Third pole environment(TPE).Environ Dev,2012,3:52-64
25 Sun H L,Zheng D,Yao T D,et al.Protection and construction of the national ecological security shelter zone on Tibetan Plateau(in Chinese).Acta Geogr Sin,2012,67:3-12[孙鸿烈,郑度,姚檀栋,等.青藏高原国家生态安全屏障保护与建设.地理学报,2012,67:3-12]
26 Chu H,Sun H,Tripathi B M,et al.Bacterial community dissimilarity between the surface and subsurface soils equals horizontal differences over several kilometers in the western Tibetan Plateau.Environ Microbiol,2016,18:1523-1533
27 Duckworth J,Jager T,Ashauer R.Automated,high-throughput measurement of size and growth curves of small organisms in well plates.Sci Rep,2019,9:10
28 Yang T,Adams J M,Shi Y,et al.Soil fungal diversity in natural grasslands of the Tibetan Plateau:Associations with plant diversity and productivity.New Phytol,2017,215:756-765
29 Che R,Deng Y,Wang F,et al.Autotrophic and symbiotic diazotrophs dominate nitrogen-fixing communities in Tibet grassland soils.Sci Total Environ,2018,639:997-1006
30 Zhang J,Wang F,Che R,et al.Precipitation shapes communities of arbuscular mycorrhizal fungi in Tibet alpine steppe.Sci Rep,2016,6:23488
31 Hijmans R J,Cameron S E,Parra J L,et al.Very high resolution interpolated climate surfaces for global land areas.Int J Climatol,2005,25:1965-1978
32 Delgado-Baquerizo M,Maestre F T,Reich P B,et al.Carbon content and climate variability drive global soil bacterial diversity patterns.Ecol Monogr,2016,86:373-390
33 Li Y,Lin Q,Wang S,et al.Soil bacterial community responses to warming and grazing in a Tibet alpine meadow.FEMS Microbiol Ecol,2016:fiv152
34 Spehn E M,Joshi J,Schmid B,et al.Plant diversity effects on soil heterotrophic activity in experimental grassland ecosystems.Plant Soil,2000,224:217-230
35 Weidner S,Koller R,Latz E,et al.Bacterial diversity amplifies nutrient-based plant-soil feedbacks.Funct Ecol,2015,29:1341-1349
36 Prober S M,Leff J W,Bates S T,et al.Plant diversity predicts beta but not alpha diversity of soil microbes across grasslands worldwide.Ecol Lett,2015,18:85-95
37 Lange M,Habekost M,Eisenhauer N,et al.Biotic and abiotic properties mediating plant diversity effects on soil microbial communities in an experimental grassland.PLo S One,2014,9:e96182
38 Hooper D U,Bignell D E,Brown V K,et al.Interactions between aboveground and belowground biodiversity in terrestrial ecosystems:Patterns,mechanisms,and feedbacks.Bio Science,2000,50:1049-1061
39 Wardle D A.The influence of biotic interactions on soil biodiversity.Ecol Lett,2006,9:870-886
40 Millard P,Singh B K.Does grassland vegetation drive soil microbial diversity?Nutr Cycl Agroecosyst,2010,88:147-158
41 Eisenhauer N,Milcu A,Sabais A C W,et al.Plant diversity surpasses plant functional groups and plant productivity as driver of soil biota in the long term.PLo S One,2011,6:e16055
42 Woodward F I,Cramer W.Plant functional types and climatic change:Introduction.J Veg Sci,1996,7:306-308
43 Bonet A.Secondary succession of semi-arid Mediterranean old-fields in south-eastern Spain:Insights for conservation and restoration of degraded lands.J Arid Environ,2004,56:213-233
44 Pausas J G,Austin M P.Patterns of plant species richness in relation to different environments:An appraisal.J Veg Sci,2001,12:153-166
45 Mayfield M M,Levine J M.Opposing effects of competitive exclusion on the phylogenetic structure of communities.Ecol Lett,2010,13:1085-1093
46 Rosindell J,Hubbell S P,He F,et al.The case for ecological neutral theory.Trends Ecol Evol,2012,27:203-208
47 Dini-Andreote F,Stegen J C,van Elsas J D,et al.Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession.Proc Natl Acad Sci USA,2015,112:E1326-E1332
48 Zhou J,Ning D.Stochastic community assembly:Does it matter in microbial ecology?Microbiol Mol Biol Rev,2017,81:e00002
49 Kang S,Xu Y,You Q,et al.Review of climate and cryospheric change in the Tibetan Plateau.Environ Res Lett,2010,5:015101
50 Xu Z X,Gong T L,Li J Y.Decadal trend of climate in the Tibetan Plateau-Regional temperature and precipitation.Hydrol Process,2008,22:3056-3065
51 Kuang X,Jiao J J.Review on climate change on the Tibetan Plateau during the last half century.J Geophys Res Atmos,2016,121:3979-4007
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