Strong functional stability of soil microbial communities under semiarid Mediterranean conditions and subjected to long-term shifts in baseline precipitation

Soil Biology and Biochemistry

Volumn 69, Issue , 2014, Pages 223-233

  Curiel Yuste, J ^a,b   Fernandez Gonzalez, A J ^c   Fernandez Lopez, M ^c   Ogaya, R ^b,d   Penuelas, J ^b,d   Sardans, J ^b,d   Lloret, F ^b  

^a MUSEO NACIONAL DE CIENCIAS NATURALES   (Spain)

^b CREAF   (Spain)

^c CSIC   (Spain)

^d CSIC   (Spain)

Author keywords

Adaptation; Diversity; Extreme events; Functional stability; Mediterranean climate; Soil bacterial communities

Indexed keywords

BACTERIA; CLIMATOLOGY; FORESTRY; SOIL MOISTURE;

ADAPTATION; DIVERSITY; EXTREME EVENTS; MEDITERRANEAN CLIMATES; SOIL BACTERIAL COMMUNITY;

DROUGHT;

ADAPTATION; BACTERIUM; CARBON DIOXIDE; DECIDUOUS FOREST; DROUGHT RESISTANCE; ECOSYSTEM FUNCTION; MEDITERRANEAN ENVIRONMENT; MICROBIAL COMMUNITY; MICROBIAL ECOLOGY; OLIGOTROPHIC ENVIRONMENT; PHENOTYPE; PHENOTYPIC PLASTICITY; PHYLOGENETICS; PRECIPITATION (CLIMATOLOGY); SEMIARID REGION; SOIL ECOSYSTEM; SOIL MICROORGANISM; WATER AVAILABILITY;

EID: 84890086324     PISSN: 00380717     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.soilbio.2013.10.045     Document Type: Article

References (73)

1. Acosta-Martinez V., Dowd S., Sun Y., Allen V. Tag-encoded pyrosequencing analysis of bacterial diversity in a single soil type as affected by management and land use. Soil Biol. Biochem. 2008, 40:2762-2770.
2. Achtman M., Wagner M. Microbial diversity and the genetic nature of microbial species. Nat. Rev. Micro. 2008, 6:431-440.
3. Acinas S.G., Sarma-Rupavtarm R., Klepac-Ceraj V., Polz M.F. PCR-induced sequence artifacts and bias: insights from comparison of two 16s rrna clone libraries constructed from the same sample. Applied and Environmental Microbiology 2005, 71:8966-8969.
4. Aelion C.M., Bradley P.M. Aerobic biodegradation potential of subsurface microorganisms from a jet fuel-contaminated aquifer. Appl. Environ. Microbiol. 1991, 57:57-63.
5. Aerts R. The freezer defrosting: global warming and litter decomposition rates in cold biomes. J.Ecol. 2006, 94:713-724.
6. Allison S.D., Martiny J.B.H. Resistance, resilience, and redundancy in microbial communities. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:11512-11519.
7. 2 exchange rates in a Mediterranean holm oak forest and their responses to drought conditions. Atmos. Environ. 2007, 41:2447-2455.
8. 2 efflux. Plant and Soil 2012, 360:163-174.
9. Baker G.C., Smith J.J., Cowan D.A. Review and re-analysis of domain-specific 16S primers. Journal of Microbiological Methods 2003, 55:541-555.
10. Balser T.C., Wixon D.L. Investigating biological control over soil carbon temperature sensitivity. Glob. Change Biol. 2009, 15:2935-2949.
11. Binladen J., Gilbert M.T.P., Bollback J.P., Panitz F., Bendixen C., et al. The use of coded pcr primers enables high-throughput sequencing of multiple homolog amplification products by 454 parallel sequencing. PLoS ONE 2007, 2(2):e197.
12. Bond-Lamberty B., Wang C.K., Gower S.T. Aglobal relationship between the heterotrophic and autotrophic components of soil respiration?. Glob. Change Biol. 2004, 10:1756-1766.
13. Carnicer J., Coll M., Ninyerola M., Pons X., SÃinchez G., Peñuelas J. Widespread crown condition decline, food web disruption, and amplified tree mortality with increased climate change-type drought. Proceedings of the National Academy of Sciences 2011, 108:1474-1478.
14. Castro H.F., Classen A.T., Austin E.E., Norby R.J., Schadt C.W. Soil Microbial community responses to multiple experimental climate change drivers. Appl. Environ. Microbiol. 2010, 76:999-1007.
15. Chao A., Chazdon R.L., Colwell R.K., Shen T.-J. Abundance-based similarity indices and their estimation when there are unseen species in samples. Biometrics 2006, 62:361-371.
16. Cole J.R., Chai B., Farris R.J., Wang Q., Kulam-Syed-Mohideen A.S., McGarrell D.M., Bandela A.M., Cardenas E., Garrity G.M., Tiedje J.M. The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data. Nucleic Acids Res. 2007, 35:D169-D172.
17. Cole J.R., Wang Q., Cardenas E., Fish J., Chai B., Farris R.J., Kulam-Syed-Mohideen A.S., McGarrell D.M., Marsh T., Garrity G.M., Tiedje J.M. The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 2009, 37:D141-D145.
18. Cruz-Martínez K., Suttle B.K., Brodie E.L., Power M.E., Andersen G.L., Banfield J.F. Despite strong seasonal responses, soil microbial consortia are more resilient to long-term changes in rainfall than overlying grassland. ISME J. 2009, 3:738-744.
19. 2 efflux. Biogeochemistry 2010, 98:127-138.
20. Curiel Yuste J.C., Baldocchi D.D., Gershenson A., Goldstein A., Misson L., Wong S. Microbial soil respiration and its dependency on carbon inputs, soil temperature and moisture. Glob. Change Biol. 2007, 13:2018-2035.
21. Curiel Yuste J.C., Penuelas J., Estiarte M., Garcia-Mas J., Mattana S., Ogaya R., Pujol M., Sardans J. Drought-resistant fungi control soil organic matter decomposition and its response to temperature. Glob. Change Biol. 2011, 17:1475-1486.
22. Curiel Yuste J., Barba J., Fernandez-Gonzalez M., Fernandez-Lopez A.J., Mattana S., Martinez-Vilalta J., Nolis P., Lloret F. Changes in soil bacterial community triggered by drought-induced gap succession preceded changes in soil C stocks and quality. Ecol. Evol. 2012, 2:3016-3031.
23. Davidson E.A., Janssens I.A. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 2006, 440:165-173.
24. Doolittle W.F., Papke R.T. Genomics and the bacterial species problem. Genome Biol. 2006, 7:116.
25. Edgar R.C., Haas B.J., Clemente J.C., Quince C., Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 2011, 27:2194-2200.
26. Excoffier L., Smouse P.E., Quattro J.M. Analysis of molecular variance inferred from metric distances among dna haplotypes - application to human mitochondrial-dna restriction data. Genetics 1992, 131:479-491.
27. Fierer N., Bradford M.A., Jackson R.B. Toward an ecological classification of soil bacteria. Ecology 2007, 88:1354-1364.
28. Fierer N., Jackson R.B. The diversity and biogeography of soil bacterial communities. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:626-631.
29. Finlay B.J., Fenchel T. Cosmopolitan metapopulations of free-living microbial eukaryotes. Protist 2004, 155:237-244.
30. Foesel B.U., Nägele V., Naether A., Wüst P.K., Weinert J., Bonkowski M., Lohaus G., Polle A., Alt F., Oelmann Y., Fischer M., Friedrich M.W., Overmann J. Determinants of Acidobacteria activity inferred from the relative abundances of 16S rRNA transcripts in German grassland and forest soils. Environ. Microbiol. 2013, http://dx.doi.org/10.1111/1462-2920.12162.
31. Fraser C., Hanage W.P., Spratt B.G. Recombination and the Nature of Bacterial Speciation. Science 2007, 315:476-480.
32. Gibelin A.L., Deque M. Anthropogenic climate change over the Mediterranean region simulated by a global variable resolution model. Clim. Dyn. 2003, 20:327-339.
33. IPCC Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change 2007, Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA. S. Solomon, D. Qin, M. Manning, Z. Chen, M. Marquis, K.B. Averyt, M.Tignor, H.L. Miller (Eds.).
34. Jones R.T., Robeson M.S., Lauber C.L., Hamady M., Knight R., Fierer N. Acomprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. Isme J. 2009, 3:442-453.
35. Lamar R.T., Dietrich D.M. Insitu depletion of pentachlorophenol from contaminated soil by phanerochaete spp. Appl. Environ. Microbiol. 1990, 56:3093-3100.
36. Landesman W.J., Dighton J. Response of soil microbial communities and the production of plant-available nitrogen to a two-year rainfall manipulation in the New Jersey Pinelands. Soil Biol. Biochem. 2010, 42:1751-1758.
37. Larcher W. Temperature stress and survival ability of Mediterranean sclerophyllous plants. Plant Biosyst. 2000, 134:279-295.
38. Lau J.A., Lennon J.T. Rapid responses of soil microorganisms improve plant fitness in novel environments. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:14058-14062.
39. Lauber C.L., Hamady M., Knight R., Fierer N. Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl. Environ. Microbiol. 2009, 75:5111-5120.
40. Lozupone C., Knight R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl. Environ. Microbiol. 2005, 71:8228-8235.
41. Margesin R., Neuner G., Storey K.B. Cold-loving microbes, plants, andanimals-fundamental and applied aspects. Naturwissenschaften 2007, 94:77-99.
42. Methe B.A., Nelson K.E., Deming J.W., Momen B., Melamud E., Zhang X.J., Moult J., Madupu R., Nelson W.C., Dodson R.J., Brinkac L.M., Daugherty S.C., Durkin A.S., DeBoy R.T., Kolonay J.F., Sullivan S.A., Zhou L.W., Davidsen T.M., Wu M., Huston A.L., Lewis M., Weaver B., Weidman J.F., Khouri H., Utterback T.R., Feldblyum T.V., Fraser C.M. The psychrophilic lifestyle as revealed by the genome sequence of Colwellia psychrerythraea 34H through genomic and proteomic analyses. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:10913-10918.
43. Nacke H., Thürmer A., Wollherr A., Will C., Hodac L., Herold N., Schöning I., Schrumpf M., Daniel R. Pyrosequencing-based assessment of bacterial community structure along different management types in German forest and grassland soils. Plos One 6 2011.
44. Nawrocki E.P., Eddy S.R. Query-dependent banding (QDB) for faster RNA similarity searches. Plos Comput. Biol. 2007, 3:540-554.
45. Ogaya R., Penuelas J. Tree growth, mortality, and above-ground biomass accumulation in a holm oak forest under a five-year experimental field drought. Plant Ecol. 2007, 189:291-299.
46. Ogaya R., Penuelas J., Asensio D., Llusia J. Chlorophyll fluorescence responses to temperature and water availability in two co-dominant Mediterranean shrub and tree species in a long-term field experiment simulating climate change. Environ. Exp. Bot. 2011, 71:123-127.
47. Pausas J.G., Verdú M. Fire reduces morphospace occupation in plant communities. Ecology 2008, 89:2181-2186.
48. Peay K.G., Kennedy P.G., Davies S.J., Tan S., Bruns T.D. Potential link between plant and fungal distributions in a dipterocarp rainforest: community and phylogenetic structure of tropical ectomycorrhizal fungi across a plant and soil ecotone. New Phytol. 2010, 185:529-542.
49. Placella S.A., Brodie E.L., Firestone M.K. Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groups. Proceedings of the National Academy of Sciences 2012, 109:10931-10936.
50. Rey A., Jarvis P. Modelling the effect of temperature on carbon mineralization rates across a network of European forest sites (FORCAST). Glob. Change Biol. 2006, 12:1894-1908.
51. Roesch L.F., Fulthorpe R.R., Riva A., Casella G., Hadwin A.K.M., Kent A.D., Daroub S.H., Camargo F.A.O., Farmerie W.G., Triplett E.W. Pyrosequencing enumerates and contrasts soil microbial diversity. Isme J. 2007, 1:283-290.
52. Sambrook J., Fritsch E.F., Maniatis T. Molecular Cloning, a Laboratory Manual 1989, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, Sect 6 1-6 19. second ed.
53. Sardans J., Penuelas J. Drought decreases soil enzyme activity in a Mediterranean Quercus ilex L. forest. Soil Biol. Biochem. 2005, 37:455-461.
54. Sardans J., Penuelas J., Ogaya R. Experimental drought reduced acid and alkaline phosphatase activity and increased organic extractable P in soil in a Quercus ilex Mediterranean forest. Eur. J. Soil Biol. 2008, 44:509-520.
55. Sardans J., Peñuelas J. Soil enzyme activity in a Mediterranean forest after six years of drought. Soil Sci. Soc. Am. J. 2010, 74:838-851.
56. Schroter D., Cramer W., Leemans R., Prentice I.C., Araujo M.B., Arnell N.W., Bondeau A., Bugmann H., Carter T.R., Gracia C.A., de la Vega-Leinert A.C., Erhard M., Ewert F., Glendining M., House J.I., Kankaanpaa S., Klein R.J.T., Lavorel S., Lindner M., Metzger M.J., Meyer J., Mitchell T.D., Reginster I., Rounsevell M., Sabate S., Sitch S., Smith B., Smith J., Smith P., Sykes M.T., Thonicke K., Thuiller W., Tuck G., Zaehle S., Zierl B. Ecosystem service supply and vulnerability to global change in Europe. Science 2005, 310:1333-1337.
57. Schimel J.P. Biogeochemical models: implicit vs. explicit microbiology. Global Biogeochemical Cycles in the Climate System 2001, 177-183. Academic Press. E.D. Schulze, S.P. Harrison, M. Heimann, E.A. Holland, J.J. LLoyd, I.C. Prentice, D. Schimel (Eds.).
58. Shade A., Peter H., Allison S.D., Baho D., Berga M., Buergmann H., Huber D.H., Langenheder S., Lennon J.T., Martiny J.B.H., Matulich K.L., Schmidt T.M., Handelsman J. Fundamentals of microbial community resistance and resilience. Front. Microbiol. 2012, 3.
59. Smit E., Leeflang P., Gommans S., van den Broek J., van Mil S., Wernars K. Diversity and seasonal fluctuations of the dominant members of the bacterial soil community in a wheat field as determined by cultivation and molecular methods. Appl. Environ. Microbiol. 2001, 67:2284-2291.
60. Specht R.L., Moll E.J. Mediterranean-type heathlands and sclerophyllous shrublands of the world - an overview. Ecol. Stud. 1983, 43:41-65.
61. Torres-Cortés G., Millán V., Fernández-González A.J., et al. Bacterial community in the rhizosphere of a cactus species during dry and rainy seasons assessed by deep sequencing. Plant Soil 2012, 357:275-288.
62. Verdu M., Pausas J.G. Fire drives phylogenetic clustering in Mediterranean Basin woody plant communities. J.Ecol. 2007, 95:1316-1323.
63. Waldrop M.P., Firestone M.K. Response of microbial community composition and function to soil climate change. Microb. Ecol. 2006, 52:716-724.
64. Waldrop M.P., Zak D.R., Blackwood C.B., Curtis C.D., Tilman D. Resource availability controls fungal diversity across a plant diversity gradient. Ecol. Lett. 2006, 9:1127-1135.
65. Wang Q., Garrity G.M., Tiedje J.M., Cole J.R. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 2007, 73:5261-5267.
66. Wardle D.A. Acomparative-assessment of factors which influence microbial biomass carbon and nitrogen levels in soil. Biol. Rev. Cambr. Philos. Soc. 1992, 67:321-358.
67. Whitman W.B., Coleman D.C., Wiebe W.J. Prokaryotes: the unseen majority. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:6578-6583.
68. Wieder W.R., Bonan G.B., Allison S.D. Global soil carbon projections are improved by modelling microbial processes. Nat. Clim. Change Advance Online Publication 2013, 3:909-912.
69. Will C., Thuermer A., Wollherr A., Nacke H., Herold N., Schrumpf M., Gutknecht J., Wubet T., Buscot F., Daniel R. Horizon-Specific bacterial community composition of German grassland soils, as revealed by pyrosequencing-based analysis of 16S rRNA genes. Appl. Environ. Microbiol. 2010, 76:6751-6759.
70. Williams M.A., Rice C.W. Seven years of enhanced water availability influences the physiological, structural, and functional attributes of a soil microbial community. Appl. Soil Ecol. 2007, 35:535-545.
71. Yergeau E., Bokhorst S., Kang S., Zhou J., Greer C.W., Aerts R., Kowalchuk G.A. Shifts in soil microorganisms in response to warming are consistent across a range of Antarctic environments. ISME J. 2012, 6:692-702.
72. Zogg G.P., Zak D.R., Ringelberg D.B., White D.C., MacDonald N.W., Pregitzer K.S. Compositional and functional shifts in microbial communities due to soil warming. Soil Sci. Soc. Am. J 1997, 61:475-481.
73. Zul D., Denzel S., Kotz A., Overmann J.r Effects of plant biomass, plant diversity, and water content on bacterial communities in soil lysimeters: implications for the determinants of bacterial diversity. Appl. Environ. Microbiol. 2007, 73:6916-6929.