Biodiversity Science ›› 2013, Vol. 21 ›› Issue (4): 411-420.doi: 10.3724/SP.J.1003.2013.10033

Special Issue: Microbes Diversity

• Orginal Article • Previous Article     Next Article

Thoughts on the microbial diversity-stability relationship in soil ecosystems

Jizheng He1, *(), Jing Li1, 2, Yuanming Zheng1   

  1. 1 State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085
    2 University of Chinese Academy of Sciences, Beijing 100049
  • Received:2013-02-02 Accepted:2013-04-16 Online:2013-07-29
  • He Jizheng

The diversity-stability relationship has been a controversial topic in ecology since the 1950s. Natural ecosystems are significantly influenced by human activity, so it is necessary to explore the diversity-stability relationship in relation to environmental disturbance and loss of biodiversity. Studies on this have focused more on above-ground terrestrial ecosystem, and consequently below-ground ecosystem has tended to be neglected, especially with regard to soil microbial diversity and stability. However, soil microbial diversity is crucial to the maintenance of ecosystem functioning as soil microorganisms influence many ecosystem processes and drive biogeochemical cycles. One important aim of soil microbial diversity research is to clarify the responses of soil microorganisms to various environmental fluctuations, so as to predict ecosystem stability and ecological service function. In this paper, we briefly introduce the concepts and research approaches for examining soil microbial diversity and below-ground ecosystem stability. Furthermore, we probe into the soil microbial diversity-stability relationship. We propose that the soil microbial system is a dynamic self-organized system. It maintains its relative stability as a result of soil microbes genetically adapting to environmental disturbances through mutation. In this way, the soil microbial system becomes resistant and resilient to environmental change and consequently sustains the stability of soil ecosystems. Future emphasis in the study of the relationships between soil microbial diversity and stability should put in the coupling processes of the below-ground ecosystem and the above-ground ecosystem. It is essential to construct a theoretical framework for soil microbial ecology by learning from theories of macroscopic ecology. We need to develop some mechanistic models to quantitatively describe and predict the relationship between soil microbial diversity and ecosystem stability.

Key words: diversity-stability, soil microorganisms, multifunctionality, functional redundancy, heredity and mutation, mechanistic model

Fig. 1

Basic framework and approaches for the study of soil microbial diversity (He & Zhang, 2011)"

Table 1

Calculations of resistance and resilience indices"

Fig. 2

Conceptual model of soil microbial system adapted to the environmental disturbance. Initial microbial community shifted to adapt to the changing environment. The number of high resistance and high resilience cluster (▲) increased to sustain the functional stability of community after the disturbance. The number of high resistance and low resilience cluster (△) maintained constant due to the high resistance. The number of low resistance and high resilience cluster (○) decreased due to the low resistance. Since the low resistance and low resilience cluster (●) did not adapt to the stress, its number sharply decreased. Stressed microbial community gradually adapted to the disturbance to form a new stable community. In this new community, the number of high resistance and high resilience cluster (▲) are the predominant species which substituted the extinctive species to sustain the functional stability of community (functional redundancy). The high resistance and low resilience cluster (△) maintained constant. The number of low resistance and high resilience cluster (○) returned to the initial status due to its high resilience in a short term. The low resistance and resilience cluster (●) disappeared and replaced by the new mutant species. After the disturbance finished, a new stable microbial community might return to the initial community."

52 van Ruijven J, Berendse F (2010) Diversity enhances community recovery, but not resistance, after drought. Journal of Ecology, 98, 81-86.
53 Ventura M, Perozzi G (2011) Introduction to the special issue “Probiotic bacteria and human gut microbiota”.Genes and Nutrition, 6, 203-204.
54 Wang GH (王国宏) (2002) Further thoughts on diversity and stability in ecosystems.Biodiversity Science(生物多样性), 10, 126-134. (in Chinese with English abstract)
55 Wertz S, Degrange V, Prosser JI, Poly F, Commeaux C, Guillaumaud N, Roux XL (2007) Decline of soil microbial diversity does not influence the resistance and resilience of key soil microbial functional groups following a model disturbance.Environmental Microbiology, 9, 2211-2219.
56 Wittebolle L, Marzorati M, Clement L, Balloi A, Daffonchio D, Heylen K, De Vos P, Verstraete W, Boon N (2009) Initial community evenness favours functionality under selective stress.Nature, 458, 623-626.
57 Wohl DL, Arora S, Gladstone JR (2004) Functional redundancy supports biodiversity and ecosystem function in a closed and sonstant environment.Ecology, 85, 1534-1540.
58 Worm B, Barbier EB, Beaumont N, Duffy JE, Floke C, Halpern BS, Jackson JBC, Lotze HK, Micheli F, Palumbi SR, Sala E, Selkoe KA, Stachowicz JJ, Watson R (2006) Impacts of biodiversity loss on ocean ecosystem services.Science, 314, 787-790.
59 Wu JF (吴建峰), Lin XG (林先贵) (2003) Effects of soil microbes on plant growth.Soils(土壤), 1, 18-21. (in Chinese with English abstract)
60 Yachi S, Loreau M (1999) Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis.Proceedings of the National Academy of Sciences,USA, 96, 1463-1468.
1 Allison G (2004) The influence of species diversity and stress intensity on community resistance and resilience.Ecological Monographs, 74, 117-134.
2 Allison SD, Martiny JBH (2008) Resistance, resilience, and redundancy in microbial communities. Proceedings of the National Academy of Sciences,USA, 105, 11512-11519.
3 Berga M, Székely AJ, Langenheder S (2012) Effects of disturbance intensity and frequency on bacterial community composition and function.PLoS ONE, 7, e36959.
4 Caporaso JG, Paszkiewicz K, Field D, Knight R, Gilbert JA (2011) The Western English Channel contains a persistent microbial seedbank.International Society for Microbial Ecology, 6, 1089-1093.
5 Chaer G, Fernandes M, Myrold D, Bottomley P (2009) Comparative resistance and resilience of soil microbial communities and enzyme activities in adjacent native forest and agricultural soils.Microbial Ecology, 58, 414-424.
6 Chen RR (陈瑞蕊), Lin XG (林先贵), Shi YQ (施亚琴) (2003) Research advances of orchid mycorrhizae.Chinese Journal of Applied Environmental Biology(应用与环境生物学报), 9, 97-101. (in Chinese with English abstract)
7 Chen SB (陈圣宾), Ouyang ZY (欧阳志云), Xu WH (徐卫华), Xiao Y (肖燚) (2010) A review of beta diversity studies.Biodiversity Science(生物多样性), 18, 323-335. (in Chinese with English abstract)
8 Copley J (2000) Ecology goes underground.Nature, 406, 452-454.
9 Creamer RE, Brennan F, Fenton O, Healy MG, Lalor STJ, Lanigan GJ, Regan JT, Griffiths BS (2010) Implications of the proposed Soil Framework Directive on agricultural systems in Atlantic Europe—a review.Soil Use and Management, 26, 198-211.
10 Cohan FM (2002) What are bacterial species? Annual Review of Microbiology, 56, 457-487.
11 Comte J, del Giorgio PA (2010) Linking the patterns of change in composition and function in bacterioplankton successions along environmental gradients.Ecology, 91, 1466-1476.
12 Didier LB, Hannes P, Lars JT (2012) Resistance and resilience of microbial communities temporal and spatial insurance against perturbations.Environmental Microbiology, 14, 2283-2292.
13 Downing AL, Leibold MA (2010) Species richness facilitates ecosystem resilience in aquatic food webs.Freshwater Biology, 55, 2123-2137.
14 Elton CS (1958) The Ecology of Invasions by Animals and Plants, pp. 143-153. Chapman Hall, London.
15 Flöder S, Jaschinski S, Wells G, Burns CW (2010) Dominance and compensatory growth in phyto-plankton communities under salinity stress.Journal of Experimental Marine Biology and Ecology, 395, 223-231.
16 Gardiner GE, Casey PG, Casey G, Lynch PB, Lawlor PG, Hill C, Fitzgerald GF, Stanton C, Ross RP (2004) Relative ability of orally administered Lactobacillus murinus to predominate and persist in the porcine gastrointestinal tract.Applied and Environmental Microbiology, 70, 1895-1906.
17 Gamfeldt L, Hillebrand H, Jonsson PR (2008) Multiple functions increase the importance of biodiversity for overall ecosystem functioning.Ecology, 89, 1223-1231.
18 Gilbert JA, Field D, Swift P, Thomas S, Cummings D, Temperton B, Weynberg K, Huse S, Hughes M, Joint I, Somerfield PJ, Mühling M (2010) The taxonomic and functional diversity of microbes at a temperate coastal site: a ‘multi-omic’ study of seasonal and diel temporal variation.PLoS ONE, 5, e15545.
19 Griffiths BS, Bonkowski M, Roy J, Ritz K (2001) Functional stability, substrate utilisation and biological indicators of soils following environmental impacts.Applied Soil Ecology, 16, 49-61.
20 Griffiths BS, Philippot L (2012) Insights into the resistance and resilience of the soil microbial community.FEMS Microbiology Review, doi:10.1111/j.1574-6976.2012. 00343. X
21 Griffiths BS, Ritz K, Bardgett RD, Cook R, Christensen S, Ekelund F, Sørensen SJ, Baath E, Bloem J, De Ruiter PC, Dolfing J, Nicolardot B (2000) Ecosystem response of pasture soil communities to fumigation induced microbial diversity reductions: an examination of the biodiversity- ecosystem function relationship.Oikos, 90, 279-294.
22 He JZ (贺纪正), Cao P (曹鹏), Zheng YM (郑袁明) (2013) Metabolic scaling theory and its application in microbial ecology.Acta Ecologica Sinica(生态学报), 33, 2645-2655. (in Chinese with English abstract)
23 He JZ (贺纪正), Ge Y (葛源) (2008) Recent advances in soil microbial biogeography.Acta Ecologica Sinica(生态学报), 28, 5571-5582. (in Chinese with English abstract)
24 He JZ, Ge Y, Xu ZH, Chen CR (2009) Linking soil bacterial diversity to ecosystem multifunctionality using backward- elimination boosted trees analysis.Journal of Soils and Sediments, 9, 547-554.
25 He JZ (贺纪正), Yuan CL (袁超磊), Shen JP (沈菊培), Zhang LM (张丽梅) (2012) Methods for and progress in research on soil metagenomics.Acta Pedologica Sinica(土壤学报), 49, 155-164. (in Chinese with English abstract)
26 He JZ (贺纪正), Zhang LM (张丽梅) (2011) Progress in research approaches of soil microbial ecology. In: Progress in Agricultural Microbiology Research and Industrialization (农业微生物研究与产业化进展) (eds Li J (李俊), Shen DL (沈德龙), Lin XG (林先贵)), pp. 94-108. Science Press, Beijing. (in Chinese)
27 Hector A, Bagchi R (2007) Biodiversity and ecosystem multifunctionality.Nature, 448, 188-190.
28 Huang JH (黄建辉), Han XG (韩兴国) (1995) Biodiversity and ecosystem stability.Chinese Biodiversity(生物多样性), 3, 31-37. (in Chinese with English abstract)
29 Kaufman LH (1982) Stream aufwuchs accumulation disturbance frequency and stress resistance and resilience.Oecologia, 52, 57-63.
30 Knight R, Jansson J, Field D, Fierer N, Desai N, Fuhrman JA, Hugenholtz P, van der Lelie D, Meyer F, Stevens R, Bailey MJ, Gordon JI, Kowalchuk GA, Gilbert JA (2012) Unlocking the potential of metagenomics through replicated experimental design.Nature Biotechnology, 30, 513-520.
31 Legendre P, Borcard D, Peres-Neto PR (2005) Analyzing beta diversity: partitioning the spatial variation of community composition data.Ecological Monographs, 75, 435-450.
32 Lennon JT, Martiny JBH (2008) Rapid evolution buffers ecosystem impacts of viruses in a microbial food web.Ecology Letters, 11, 1178-1188.
33 Li B (李博) (2000) Ecology (生态学), pp. 340-347. Higher Education Press, Beijing. (in Chinese)
34 Lin XG (林先贵), Hu JL (胡君利) (2008) Scientific connotation and ecological service function of soil microbial diversity.Acta Pedologica Sinica(土壤学报), 45, 892-900. (in Chinese with English abstract)
35 Litchman E (2010) Invisible invaders: non-pathogenic invasive microbes in aquatic and terrestrial ecosystems.Ecology Letters, 13, 1560-1572.
36 MacArthur R (1955) Fluctuations of animal populations, and a measure of community stability.Ecology, 36, 533-536.
37 Martiny JB, Bohannan BJ, Brown JH, Colwell RK, Fuhrman JA, Green JL, Horner-Devine MC, Kane M, Krumins JA, Kuske CR, Morin PJ, Naeem S, Ovreås L, Reysenbach AL, Smith VH, Staley JT (2006) Microbial biogeography: putting microorganisms on the map.Nature Review Microbiology, 4, 102-112.
38 McCann KS (2000) The diversity-stability debate.Nature, 405, 228-233.
39 Metchnikoff II (1908) The Nature of Man: Studies in Optimistic Philosophy. GP Putman’s Sons, New York.
40 Mercé B, Anna JS, Silke L (2012) Effects of disturbance intensity and frequency on bacterial comminuty composition and function.PLoS ONE, 7, e36959.
41 Oneill RV (1976) Ecosystem persistence and heterotrophic regulation.Ecology, 57, 1244-1253.
42 Orwin KH, Wardle DA (2004) New indices for quantifying the resistance and resilience of soil biota to exogenous disturbances.Soil Biology and Biochemistry, 36, 1907-1912.
43 Pimm SL (1984) The complexity and stability of ecosystems.Nature, 307, 321-326.
44 Prosser JI (1989) Autotrophic nitrification in bacteria.Advances in Microbial Physiology, 30, 125-181.
45 Shade A, Peter H, Allison SD, Baho D, Berga M, Buergmann H, Huber DH, Langenheder S, Lennon JT, Martiny JB, Matulich K, Schmidt TM, Handelsman J (2012) Fundamentals of microbial community resistance and resilience.Frontiers in Microbiology, 3, 417.
46 Shea K, Chesson P (2002) Community ecology theory as a frame-work for biological invasions.Trends in Ecology and Evolution, 17, 170-176.
47 Sousa WP (1980) The responses of a community to disturbance: the importance of successional age and species life history strategies.Oecologia, 45, 72-81.
48 Teeling H, Fuchs BM, Becher D, Klockow C, Gardebrecht A, Bennke CM, Kassabgy M, Huang S, Mann AJ, Waldmann J, Weber M, Klindworth A, Otto A, Lange J, Bernhardt J, Reinsch C, Hecker M, Peplies J, Bockelmann FD, Callies U, Gerdts G, Wichels A, Wiltshire KH, Glöckner FO, Schweder T, Amann R (2012) Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom.Science, 336, 608-611.
49 Tilman D (1996) Biodiversity: population versus ecosystem stability.Ecology, 77, 350-363.
50 Tilman D, Reich PB, Knops JMH (2006) Biodiversity and ecosystem stability in a decade-long grassland experiment.Nature, 441, 629-632.
51 van Elsas JD, Chiurazzi M, Mallon CA, Krištufek EV, Salles JF (2012) Microbial diversity determines the invasion of soil by a bacterial pathogen.Proceedings of the National Academy of Sciences, USA, 109, 1159-1164.
61 Zhang B, Deng H, Wang HL, Yin R, Hallett PD, Griffiths BS, Daniell TJ (2010) Does microbial habitat or community structure drive the functional stability of microbes to stresses following re-vegetation of a severely degraded soil? Soil Biology and Biochemistry, 42, 850-859.
[1] Anrong Liu,Teng Yang,Wei Xu,Zijian Shangguan,Jinzhou Wang,Huiying Liu,Yu Shi,Haiyan Chu,Jin-Sheng He. (2018) Status, issues and prospects of belowground biodiversity on the Tibetan alpine grassland . Biodiv Sci, 26(9): 972-987.
[2] Zi-Piao YE, Shi-Hua DUAN, Ting AN, Hua-Jing KANG. (2018) Determination of maximum electron transport rate and its impact on allocation of electron flow . Chin J Plan Ecolo, 42(4): 498-507.
[3] Xue-Mei WANG, Bang-Guo YAN, Guang ZHAO, Liang-Tao SHI, Gang-Cai LIU, Hai-Dong FANG. (2017) Effects of microorganism on carbon, nitrogen and phosphorus of Dodonaea viscosa and the soils from different elevations in Yuanmou, Yunnan, China . Chin J Plan Ecolo, 41(3): 311-324.
[4] Xiaobo Huang, Shuaifeng Li, Jianrong Su, Wande Liu, Xuedong Lang. (2017) The relationship between species richness and ecosystem multifunctionality in the Pinus yunnanensis natural secondary forest . Biodiv Sci, 25(11): 1182-1191.
[5] Lingjie Lei,Deliang Kong,Xiaoming Li,Zhenxing Zhou,Guoyong Li. (2016) Plant functional traits, functional diversity, and ecosystem functioning: current knowledge and perspectives . Biodiv Sci, 24(8): 922-931.
[6] Jing-Peng LI, Zhi-Rong ZHENG, Nian-Xi ZHAO, Yu-Bao GAO. (2016) Relationship between ecosystem multifuntionality and species diversity in grassland ecosystems under land-use types of clipping, enclosure and grazing . Chin J Plan Ecolo, 40(8): 735-747.
[7] Jing Yan,Xiaoya Zhang,Xue Chen,Yue Wang,Fengjuan Zhang,Fanghao Wan. (2016) Effects of rhizosphere soil microorganisms and soil nutrients on competitiveness of Bidens pilosa with different native plants . Biodiv Sci, 24(12): 1381-1389.
[8] Zi-Piao YE, Wen-Hai HU, Xiao-Hong YAN. (2016) Comparison on light-response models of actual photochemical efficiency in photosystem II . Chin J Plan Ecolo, 40(11): 1208-1217.
[9] Wei Xu,Xin Jing,Zhiyuan Ma,Jin-Sheng He. (2016) A review on the measurement of ecosystem multifunctionality . Biodiv Sci, 24(1): 72-84.
[10] Wei Xu,Zhiyuan Ma,Xin Jing,Jin-Sheng He. (2016) Biodiversity and ecosystem multifunctionality: advances and perspectives . Biodiv Sci, 24(1): 55-.
[11] LI Xiao-Rong, WEI Jin-Yu, CHEN Yun, CAO Ting-Ting, FENG Li, GU Mei-Zi, LI Lei. (2014) Functional diversity of soil microorganisms in Casuarina equisetifolia woodlands of different stand ages in Hainan Island . Chin J Plan Ecolo, 38(6): 608-618.
[12] YE Zi-Piao, HU Wen-Hai, XIAO Yi-An, FAN Da-Yong, YIN Jian-Hua, DUAN Shi-Hua, YAN Xiao-Hong, HE Li, and ZHANG Si-Si. (2014) A mechanistic model of light-response of photosynthetic electron flow and its application . Chin J Plan Ecolo, 38(11): 1241-1249.
[13] SUN Yue, XU Xing-Liang, and Yakov KUZYAKOV. (2014) Mechanisms of rhizosphere priming effects and their ecological significance . Chin J Plan Ecolo, 38(1): 62-75.
[15] Zhenguo Liu, Zhenqing Li, Ming Dong. (2005) Model analysis of plant community dynamics . Biodiv Sci, 13(3): 269-277.
Full text