Abstract
Water and nutrient availability are the major limiting factors of biological activity in arid and semiarid ecosystems. Therefore, perennial plants have developed different ecophysiological adaptations to cope with harsh conditions. The chemical profile of the root exudates varies among plant species and this can induce variability in associated microbial populations. We examined the influence of two shrubs species, Artemisia sieberi and Noaea mucronata, on soil microbial diversity. Soil samples were collected monthly, from December 2006 to November 2007, near canopies of both shrubs (0–10-cm depth). Samples were used for abiotic tests and determination of soil bacterial diversity. No significant differences were found in the abiotic variables (soil moisture, total organic matter, and total soluble nitrogen (TSN)) between soil samples collected from under the two shrubs during the study period. No obvious differences in the Shannon–Weaver index, evenness values, or total phylogenetic distances were found for the soil microbial communities. However, detailed denaturing gradient gel electrophoresis (DGGE) clustering as well as taxonomic diversity analyses indicated clear shifts in the soil microbial community composition. These shifts were governed by seasonal variability in water availability and, significantly, by plant species type.
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References
Noy-Meir I (1973) Desert ecosystems: environment and producers. Ann Rev Ecol Syst 4:25–51
Noy-Meir I (1974) Desert ecosystems: higher trophic levels. Ann Rev Ecol Syst 5:195–214
West NE, Skujins J (1978) Nitrogen in desert ecosystems, US/IBP no. 9. Dowden, Hutchinson and Ross, Stroudsburg
Larson WE, Pierce FJ (1994) The dynamics of soil quality as measure of sustainable management. In: Doran DW, Coleman DC, Bendicek DF, Stewart BA (eds) Defining soil quality for sustainable environment. Soil Science Society of America Inc. and American Society of Agronomy Inc., Madison, pp 37–51
Steinberger Y, Loboda I (1991) Nematode population dynamics and trophic structure in a soil profile under the canopy of the desert shrub Zygophyllum dumosum. Pedobiologia 35:191–197
Steinberger Y (1995) Soil fauna in arid ecosystems: their role and functions in organic matter cycling. Adv GeoEcol 28:29–36
Cornwell WK, Cornelissen JHC, Amatangelo K, Dorrepaal E, Eviner VT, Godoy O, Hobbie SE, Hoorens B, Kurokawa H, Perez-Harguindeguy N, Quested HM, Santiago LS, Wardle DA, Wright IJ, Aerts R, Allison SD, van Bodegom P, Brovkin V, Chatain A, Callaghan TV, Diaz S, Garnier E, Gurvich DE, Kazakou E, Klein JA, Read J, Reich PB, Soudzilovskaia NA, Vaieretti MV, Westoby M (2008) Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecol Lett 11:1065–1071
Buyanovsky G, Dicke M, Berwick P (1982) Soil environment and activity of soil microflora in the Negev Desert. J Arid Environ 5:13–28
Coleman DC (1985) Through a ped darkly: an ecological assessment of root-soil-microbial-faunal interactions. In: Fitter AH, Atkinson D, Read DJ, Usher MB (eds) Ecological interactions in soil. Blackwell, Cambridge, pp 1–21
Beare MH, Parmelee RW, Hendrix PF, Cheng W (1992) Microbial and fungal interactions and effects on litter nitrogen and decomposition in agroecosystems. Ecol Monogr 62:569–591
Sarig S, Steinberger Y (1993) Immediate effect of wetting event on microbial biomass and carbohydrate production mediated aggregation in desert soil. Geoderma 56:599–607
Evenari ME, Shanan L, Tadmor W (1982) The Negev: the challenge of a desert. Harvard University Press, Cambridge
Shmida A, Evenari M, Noy-Meir I (1986) Hot desert ecosystems. An integrated view. In: Evenari M, Noy-Meir I, Goodall DW (eds) Ecosystems of the world: hot deserts and arid shrublands. Elsevier, Amsterdam, pp 379–387
Whitford WG (2002) Ecology of desert systems. Academic, New York
Zhou JZ, Davey ME, Figueras JB, Rivkina E, Gilichinsky D, Tiedje JM (1997) Phylogenetic diversity of a bacterial community determined from Siberian tundra soil DNA. Microbiology 143:3913–3919
Bagayoko M, Alvey S, Neumann G, Buerkert A (2000) Root-induced increases in soil pH and nutrient availability to field-grown cereals and legumes on acid sandy soils of Sudano-Sahelian West Africa. Plant Soil 225:117–127
Stephan A, Meyer AH, Schmid B (2000) Plant diversity affects culturable soil bacteria in experimental grassland communities. J Ecol 88:988–998
Smalla K, Wieland G, Buchner A, Zock A, Parzy J, Kaiser S, Roskot N, Heuer H, Berg G (2001) Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microbiol 67:4742–4751
Costa R, Gotz M, Mrotzek N, Lottmann J, Berg G, Smalla K (2006) Effects of site and plant species on rhizosphere community structure as revealed by molecular analysis of microbial guilds. FEMS Microbiol Ecol 56:236–249
Loranger-Merciris G, Barthes L, Gastine A, Leadley P (2006) Rapid effects of plant species diversity and identity on soil microbial communities in experimental grassland ecosystems. Soil Biol Biochem 38:2336–2343
McCaig AE, Glover LA, Prosser JI (1999) Molecular analysis of bacterial community structure and diversity in unimproved and improved upland grass pastures. Appl Environ Microbiol 65:1721–1730
Kowalchuk GA, Buma DS, de Boer W, Klinkhamer PGL, van Veen JA (2002) Effects of above-ground plant species composition and diversity on the diversity of soil-borne microorganisms. Anton Leeuw Int J G 81:509–520
Nunan N, Daniell TJ, Singh BK, Papert A, McNicol JW, Prosser JI (2005) Links between plant and rhizoplane bacterial communities in grassland soils, characterized using molecular techniques. Appl Environ Microbiol 71:6784–6792
Haichar FE, Marol C, Berge O, Rangel-Castro JI, Prosser JI, Balesdent J, Heulin T, Achouak W (2008) Plant host habitat and root exudates shape soil bacterial community structure. ISME J 2:1221–1230
Sorensen J (1997) The rhizosphere as a habitat for soil microorganisms. In: van Elsas JD, Trevors JT, Wellington EMH (eds) Modern soil microbiology. Marcel Dekker, New York, pp 21–45
Jaeger CH, Lindow SE, Miller S, Clark E, Firestone MK (1999) Mapping of sugar and amino acid availability in soil around roots with bacterial sensors of sucrose and Tryptophan. Appl Environ Microbiol 65:2685–2690
Lynch JM, Whipps JM (1990) Substrate flow in the rhizosphere. Plant Soil 129:1–10
Friedman J (1995) Allelopathy, autotoxicity, and germination. In: Kigel J, Galili G (eds) Seed development and germination. Marcel Dekker, NY, pp 599–628
Rowell DL (1994) Soil science: methods and applications. Longman, London
Lahav I, Steinberger Y (2001) Soil bacterial functional diversity in a potato field. Eur J Soil Biol 37:59–67
S.F.A.S. (1995) Manual—SAN Plus analyzer. Skalar Analytical, The Netherlands
Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Sun S, Chen J, Li W, Altinatas I, Lin A, Peltier S, Stocks K, Allen EE, Ellisman M, Grethe J, Wooley J (2011) Community cyberinfrastructure for advanced microbial ecology research and analysis: the CAMERA resource. Nucleic Acids Res 39(Suppl 1):D546–D551
Shannon CE, Weaver W (1949) The mathematical theory of communication. University of Illinois Press, Urbana
Pielou EC (1966) The measurement of diversity in different types of biological collections. Statistical Research Service, Canada Department of Agriculture, Ottawa
Sorensen T (1948) A method of establishing groups of equal amplitude in plant society based on similarity of species content. K Danske Vidensk Selsk Biol SKR 5:1–34
Huson DH, Auch AF, Qi J, Schuster SC (2007) MEGAN analysis of metagenomic data. Genome Res 17:377–386
Huson DH, Mitra S, Ruscheweyh HJ, Weber N, Schuster SC (2011) Integrative analysis of environmental sequences using MEGAN4. Genome Res 21:1552–1560
Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267
Niu B, Fu L, Sun S, Li W (2010) Artificial and natural duplicates in pyrosequencing reads of metagenomic data. BMC Bioinform 11:187
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and clustal X version 2.0. Bioinformatics 23:2947–2948
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704
Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10
Faith DP (2006) The role of the phylogenetic diversity measure, PD, in bio-informatics: getting the definition right. Evol Bioinform 2:277–283
Zhang H, Sekiguchi Y, Hanada S, Hugenholtz P, Kim H, Kamagata Y, Nakamura K (2003) Gemmatimonas aurantiaca gen. nov., sp nov., a gram-negative, aerobic, polyphosphate-accumulating micro-organism, the first cultured representative of the new bacterial phylum Gemmatimonadetes phyl. nov. Int J Syst Evol Microbiol 53:1155–1163
Martin-Laurent F, Philippot L, Hallet S, Chaussod R, Germon JC, Soulas G, Catroux G (2001) DNA extraction from soils: old bias for new microbial diversity analysis methods. Appl Environ Microbiol 67:2354–2359
McGuire KL, Treseder KK (2010) Microbial communities and their relevance for ecosystem models: decomposition as a case study. Soil Biol Biochem 42:529–535
Maloney PE, van Bruggen AHC, Hu S (1997) Bacterial community structure in relation to the carbon environment in lettuce and tomato rhizosphere and in bulk soil. Microb Ecol 34:109–117
Hertenberger G, Zampach P, Bachmann G (2002) Plant species affect the concentration of free sugars and free amino acids in different types of soil. J Plant Nutr Soil Sci 165:557–565
Buckley DH, Schmidt TM (2003) Diversity and dynamics of microbial communities in soils from agro-ecosystems. Environ Microbiol 5:441–452
Johnson MJ, Lee KY, Scow KM (2003) DNA fingerprinting reveals links among agricultural crops, soil properties, and the composition of soil microbial communities. Geoderma 114:279–303
Steinberger Y, Vishnevetsky S, Barness G, Lavee H (1998) Effects of topoclimatic gradient on soil dehydrogenase activity in a Judean Desert ecosystem. Arid Soil Res Rehab 12:387–393
Dilly O, Buscot F, Varma A (2005) Microbial energetics in soils. Soil biology, volume 3, Microorganisms in soils: roles in genesis and functions. Springer, Berlin, pp 123–138
Jones DL, Murphy DV (2007) Microbial response time to sugar and amino acid additions to soil. Soil Biol Biochem 39:2178–2182
Broeckling CD, Broz AK, Bergelson J, Manter DK, Vivanco JM (2008) Root exudates regulate soil fungal community composition and diversty. Appl Environ Microbiol 74:738–744
Brimecombe MJ, De Leij FA, Lynch JA (2001) The effect of root exudates on rhizosphere microbial populations. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere: biochemistry and organic substances at the soil–plant interface. Marcel Dekker, Inc., NY, pp 95–104
Jacobson KM, Jacobson PJ (1998) Rainfall regulates decomposition of buried cellulose in the Namib Desert. J Arid Environ 38:571–583
Bachelet D, Brugnach M, Neilson RP (1998) Sensitivity of a biogeography model to soil properties. Ecol Model 109:77–98
Reynolds JF, Virginia RA, Kemp PR, de Soyza AG, Tremmel DC (1999) Impact of drought on desert shrubs: effects of seasonality and degree of resource island development. Ecol Monogr 69:69–106
Reynolds JF, Kemp PR, Ogle K, Fernandez RJ (2004) Modifying the ‘pulse-reserve’ paradigm for deserts of North America: precipitation pulses, soil water, and plant responses. Oecologia 141:194–210
Janssen PH (2006) Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 72:1719–1728
Germida JJ, Siciliano SD, de Freitas JR, Seib AM (1998) Diversity of root-associated bacteria associated with field-grown canola (Brassica napus L.) and wheat (Triticum aestivum L.). FEMS Microbiol Ecol 26:43–50
Germida JJ, Siciliano SD (2001) Taxonomic diversity of bacteria associated with the roots of modern, recent and ancient wheat cultivars. Biol Fertil Soils 33:410–415
Di Cello F, Bevivino A, Chiarini L, Fani R, Paffetti D, Tabacchioni S, Dalmastri C (1997) Biodiversity of a Burkholderia cepacia population isolated from the maize rhizosphere at different plant growth stages. Appl Environ Microbiol 63:4485–4493
Latour X, Corberand TS, Laguerre G, Allard F, Lemanceau P (1996) The composition of fluorescent pseudomonad populations associated with roots is influenced by plant and soil type. Appl Environ Microbiol 62:2449–2456
Westover KM, Kennedy AC, Kelley SC (1997) Patterns of rhizosphere microbial community structure associated with co-occurring plant species. J Ecol 85:863–873
Marschner P, Yang CH, Lieberei R, Crowley DE (2001) Soil and plant specific effects on bacterial community composition in the rhizosphere. Soil Biol Biochem 33:1437–1445
Bowen GD, Rovira AD (1991) The rhizosphere—the hidden half of the hidden half. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots—the hidden half. Marcel Dekker, New York, pp 641–649
Bolton H Jr, Fredrickson JK, Elliott LF (1994) Microbial ecology of the rhizosphere. In: Metting FB Jr (ed) Soil microbial ecology. Marcel Dekker, New York, pp 27–63
Grayston SJ, Wang S, Campbell CD, Edwards AC (1998) Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol Biochem 30:369–378
Carney KM, Matson PA (2005) Plant communities, soil microorganisms, and soil carbon cycling: does altering the world belowground matter to ecosystem functioning? Ecosystems 8:928–940
Acknowledgments
The authors thank Lilach Iasur, Hila Elifantz, and Patricia Bucki (students of Dr. Dror Minz), and Dr. Einav Mayzlish-Gati for consultation and guidance. Many thanks go to Dr. Orit Shaul for providing the necessary equipment. Special thanks to Ms. Sharon Victor for language editing.
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This paper is dedicated in loving memory to Saul Saul (father of V.S.-T.).
Subject category: Microbial population and community ecology: environmental factors (biotic and abiotic) defining the distribution and abundance of microbial populations.
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Saul-Tcherkas, V., Unc, A. & Steinberger, Y. Soil Microbial Diversity in the Vicinity of Desert Shrubs. Microb Ecol 65, 689–699 (2013). https://doi.org/10.1007/s00248-012-0141-8
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DOI: https://doi.org/10.1007/s00248-012-0141-8