Total and active microbial communities and phoD as affected by phosphate depletion and pH in soil

Springer Science and Business Media LLC - Tập 408 - Trang 15-30 - 2016
Sabine A. Ragot1,2, Olivier Huguenin-Elie3, Michael A. Kertesz4, Emmanuel Frossard1, Else K. Bünemann1,5
1Institute of Agricultural Sciences, ETH Zurich, Lindau, Switzerland
2ETH Zurich – Plant Nutrition, Lindau, Switzerland
3Agroscope, Institute of Sustainable Sciences, Zürich, Switzerland
4Centre for Carbon, Water and Food, Faculty of Agriculture and Environment, University of Sydney, Sydney, Australia
5Department of Soil Sciences, FiBL, Frick, Switzerland

Tóm tắt

Soil microbial communities contribute to organic phosphorus cycling in a variety of ways, including secretion of the PhoD alkaline phosphatase. We sampled a long-term grassland fertilization trial in Switzerland characterized by a natural pH gradient. We examined the effects of phosphate depletion and pH on total and active microbial community structures and on the structure and composition of the total and active phoD-harboring community. Archaeal, bacterial and fungal communities were investigated using T-RFLP and phoD-harboring members of these communities were identified by 454-sequencing. Phosphate depletion decreased total, resin-extractable and organic phosphorus and changed the structure of all active microbial communities, and of the total archaeal and phoD-harboring communities. Organic carbon, nitrogen and phosphorus increased with pH, and the structures of all total and active microbial communities except the total fungal community differed between the two pH levels. phoD-harboring members were affiliated to Actinomycetales, Bacilliales, Gloeobacterales, Planctomycetales and Rhizobiales. Our results suggest that pH and associated soil factors are important determinants of microbial and phoD-harboring community structures. These associated factors include organic carbon and total nitrogen, and to a lesser degree phosphorus status, and active communities are more responsive than total communities. Key players in organic P mineralization are affiliated to phyla that are known to be important in organic matter decomposition.

Tài liệu tham khảo

Alef K, Nannipieri P, Trasar-Cepeda C (1995) Phosphatase activity. In: Alef K, Nannipieri P (eds) Methods in Applied Soil Microbiology and Biochemistry. Academic Press, London Anderson JM, Ingram JSI (1993) Tropical soil biology and fertility. A handbook of methods. CAB International, Wallingford Baldrian P, Kolařík M, Štursová M, Kopecký J, Valášková V, Větrovský T, Žifčáková L, Šnajdr J, Rídl J, Vlček Č (2012) Active and total microbial communities in forest soil are largely different and highly stratified during decomposition. ISME J 6:248–258 Beauregard MS, Hamel C, Nayyar A, St-Arnaud M (2009) Long-term phosphorus fertilization impacts soil fungal and bacterial diversity but not AM fungal community in Alfalfa. Microb Ecol 59:379–389 Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13 Bissett A, Richardson AE, Baker G, Thrall PH (2011) Long-term land use effects on soil microbial community structure and function. Appl Soil Ecol 51:66–78 Blagodatskaya EV, Anderson TH (1998) Interactive effects of pH and substrate quality on the fungal-to-bacteria ratio and qCO2 of microbial communities in forest soils. Soil Biol Biochem 20:1269–1274 Bowman RA, Moir JO (1993) Basic EDTA as an extractant for soil organic phosphorus. Soil Sci Soc Am J 57:1516–1518 Buckley DH, Huangyutitham V, Hsu S-F, Nelson TA (2007) Stable isotope probing with 15N2 reveals novel noncultivated diazotrophs in soil. Appl Environ Microbiol 73:3196–3204 Bünemann EK, Marschner P, McNeill AM, McLaughlin MJ (2007) Measuring rates of gross and net mineralisation of organic phosphorus in soils. Soil Biol Biochem 39:900–913 Bünemann EK, Oberson A, Liebisch F, Keller F, Annaheim KE, Huguenin-Elie O, Frossard E (2012) Rapid microbial phosphorus immobilization dominates gross phosphorus fluxes in a grassland soil with low inorganic phosphorus availability. Soil Biol Biochem 51:84–95 Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL (2009) BLAST+: architecture and applications. BMC bioinformatics 10:421 Chao AC, Shen T-J (2003) Nonparametric estimation of Shannon's index of diversity when there are unseen species in sample. Environ Ecol Stat 10:429–443 Chhabra S, Brazil D, Morrissey J, Burke J, O’Gara F, Dowling DN (2012) Fertilization management affects the alkaline phosphatase bacterial community in barley rhizosphere soil. Biol Fertil Soils 49:31–39 Condron LM, Turner BL, Cade-Menun BJ (2005) Chemistry and dynamics of soil organic phosphorus. In: Sims JT, Sharpley AN (eds) Phosphorus: agriculture and the environment. ASA, CSSA and SSSA, Madison Cruz AF, Hamel C, Hanson K, Selles F, Zentner RP (2009) Thirty-seven years of soil nitrogen and phosphorus fertility management shapes the structure and function of the soil microbial community in a Brown Chernozem. Plant Soil 315:173–184 Cui H, Zhou Y, Gu Z, Zhu H, Fu S, Yao Q (2015) The combined effects of cover crops and symbiotic microbes on phosphatase gene and organic phosphorus hydrolysis in subtropical orchard soils. Soil Biol Biochem 82:119–126 Culman SW, Bukowski R, Gauch HG, Cadillo-Quiroz H, Buckley DH (2009) T-REX: software for the processing and analysis of T-RFLP data. BMC bioinformatics 10:171–181 Dequiedt S, Saby NPA, Lelievre M, Jolivet C, Thioulouse J, Toutain B, Arrouays D, Bispo A, Lemanceau P, Ranjard L (2011) Biogeographical patterns of soil molecular microbial biomass as influenced by soil characteristics and management. Glob Ecol Biogeogr 20:641–652 Dietl W (1995) Wandel der Wiesenvegetation im Schweizer Mittelland. Zeitschrift für Ökologie und Naturschutz 4:239–249 Drenovsky R, Vo D, Graham K, Scow K (2004) Soil water content and organic carbon availability are major determinants of soil microbial community composition. Microb Ecol 48:424–430 Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci U S A 103:626–631 Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364 Fraser T, Lynch DH, Entz MH, Dunfield KE (2015) Linking alkaline phosphatase activity with bacterial phoD gene abundance in soil from a long-term management trial. Geoderma 257:115–122 Frossard E, Brossard M, Hedley MJ, Metherell A (1995) Reactions controlling the cycling of P in soils. In: Tiessen H (ed) Phosphorus cycling in terrestrial and aquatic ecosystems: a global perspective. SCOPE/Wiley, New York Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118 Griffiths RI, Thomson BC, James P, Bell T, Bailey M, Whiteley AS (2011) The bacterial biogeography of British soils. Environ Microbiol 13:1642–1654 Hayatsu M, Tago K, Saito M (2008) Various players in the nitrogen cycle: diversity and functions of the microorganisms involved in nitrification and denitrification. Soil Sci Plant Nutr 54:33–45 He JZ, Shen JP, Zhang LM, Zhu YG, Zheng YM, Xu MG, Di H (2007) Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. Environ Microbiol 9:2364–2374 Hill MO, Mountford J, Roy D, Bunce RGH (1999) Ellenberg's indicator values for British plants. ECOFACT Volume 2 Technical Annex. Institute of Terrestrial Ecology Huguenin-Elie O, Gago R, Stutz C, Lüscher A, Kessler W (2006) Long-term effects of fertilisation on herbage composition, yield and quality of an Arrhenatherion-type meadow. Grass Sci Eur 11:550–552 Jarosch KA, Doolette AL, Smernik RJ, Tamburini F, Frossard E, Bünemann EK (2015) Characterisation of soil organic phosphorus in NaOH-EDTA extracts: A comparison of 31 P NMR spectroscopy and enzyme addition assays. Soil Biol Biochem 91:298–309 Jorquera MA, Martinez OA, Marileo LG, Acuna JJ, Saggar S, Mora ML (2014) Effect of nitrogen and phosphorus fertilization on the composition of rhizobacterial communities of two Chilean Andisol pastures. World J Microbiol Biotechnol 30:99–107 Kageyama H, Tripathi K, Rai AK, Cha-um S, Waditee-Sirisattha R, Takabe T (2011) An alkaline phosphatase/phosphodiesterase, PhoD, induced by salt stress and secreted out of the cells of Aphanothece halophytica, a halotolerant cyanobacterium. Appl Environ Microbiol 77:5178–5183 Kouno K, Tuchiya Y, Ando T (1995) Measurement of soil microbial biomass phosphorus by an anion exchange membrane method. Soil Biol Biochem 27:1353–1357 Lauber CL, Strickland MS, Bradford MA, Fierer N (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem 40:2407–2415 Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120 Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280 Lehtovirta LE, Prosser JI, Nicol GW (2009) Soil pH regulates the abundance and diversity of Group 1.1c Crenarchaeota. FEMS Microbiol Ecol 70:367–376 Liebisch F, Bünemann E, Huguenin-Elie O, Jeangros B, Frossard E, Oberson A (2013) Plant phosphorus nutrition indicators evaluated in agricultural grasslands managed at different intensities. Eur J Agron 44:67–77 Liu L, Gundersen P, Zhang TQ, Mo J (2012) Effects of phosphorus addition on soil microbial biomass and community composition in three forest types in tropical China. Soil Biol Biochem 44:31–38 Lueders T, Friedrich M (2000) Archaeal population dynamics during sequential reduction processes in rice field soil. Appl Environ Microbiol 66:2732–2742 Luo H, Benner R, Long RA, Hu J (2009) Subcellular localization of marine bacterial alkaline phosphatases. Proc Natl Acad Sci U S A 106:21219–21223 Mander C, Wakelin S, Young S, Condron L, O’Callaghan M (2012) Incidence and diversity of phosphate-solubilising bacteria are linked to phosphorus status in grassland soils. Soil Biol Biochem 44:93–101 Marx MC, Wood M, Jarvis SC (2001) A microplate fluorimetric assay for the study of enzyme diversity in soils. Soil Biol Biochem 33:1633–1640 Nacke H, Thürmer A, Wolher A, Will C, Hodac L, Herold N, Schöning I, Schrumpf M, Rolf D (2011) Pyrosequencing-based assessment of bacterial community structure alon different management types in German forest and grassland soils. PLoS One 6:e17000 Nicol GW, Leininger S, Schleper C, Prosser JI (2008) The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ Microbiol 10:2966–2978 Ohno R, Zibilske LM (1991) Determination of low concentrations of phosphorus in soil extracts using malachite green. Soil Sci Soc Am J 55:892–895 Philipp A, Huguenin-Elie O, Flisch R, Gago R, Stutz C, Kessler W (2004) Effects of phosphate input on a low input meadow. Agrarforschung Schweiz 11:86–91 Poll C, Ingwersen J, Stemmer M, Gerzabek MH, Kandeler E (2006) Mechanisms of solute transport affect small-scale abundance and function of soil microorganisms in the detritusphere. Eur J Soil Sci 57:583–595 Ragot SA, Kertesz MA, Bünemann EK (2015) phoD alkaline phosphatase gene diversity in soil. Appl Environ Microbiol 81:7281–7289 Ramette A (2007) Multivariate analyses in microbial ecology. FEMS Microbiol Ecol 62:142–160 Rousk J, Baath E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351 Sakurai M, Wasaki J, Tomizawa Y, Shinano T, Osaki M (2008) Analysis of bacterial communities on alkaline phosphatase genes in soil supplied with organic matter. Soil Sci Plant Nutr 54:62–71 Schloss PD, Larget BR, Handelsman J (2004) Integration of microbial ecology and statistics: a test to compare gene libraries. Appl Environ Microbiol 70:5485–5492 Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541 Siciliano SD, Palmer AS, Winsley T, Lamb E, Bissett A, Brown MV, van Dorst J, Ji M, Ferrari BC, Grogan P (2014) Soil fertility is associated with fungal and bacterial richness, whereas pH is associated with community composition in polar soil microbial communities. Soil Biol Biochem 78:10–20 Štursová M, Žifčáková L, Leigh MB, Burgess R, Baldrian P (2012) Cellulose utilization in forest litter and soil: identification of bacterial and fungal decomposers. FEMS Microbiol Ecol 80:735–746 Tan H, Barret M, Mooij MJ, Rice O, Morrissey JP, Dobson A, Griffiths B, O’Gara F (2013) Long-term phosphorus fertilisation increased the diversity of the total bacterial community and the phoD phosphorus mineraliser group in pasture soils. Biol Fertil Soils 49:661–672 Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707 Vershinina OA, Znamenskaya LV (2002) The Pho regulons of bacteria. Microbiology 71:497–511 Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecol Appl 20:5–15 Wakelin SA, Macdonald LM, Rogers SL, Gregg AL, Bolger TP, Baldock JA (2008) Habitat selective factors influencing the structural composition and functional capacity of microbial communities in agricultural soils. Soil Biol Biochem 40:803–813 Wang Y, Marschner P, Zhang F (2012a) Phosphorus pools and other soil properties in the rhizosphere of wheat and legumes growing in three soils in monoculture or as a mixture of wheat and legume. Plant Soil 354:283–298 Wang Y, Zhang F, Marschner P (2012b) Soil pH is the main factor influencing growth and rhizosphere properties of wheat following different pre-crops. Plant Soil 360:271–286 Westerman RL (1990) Soil testing and plant analysis. SSSA, Madison White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: A Guide to Methods and Applications 18:315–322 Winsley T, van Dorst JM, Brown MV, Ferrari BC (2012) Capturing greater 16S rRNA gene sequence diversity within the domain Bacteria. Appl Environ Microbiol 78:5938–5941 WRB (2014) World reference base for soil resources. World Soil Ressources Reports, FAO, Rome Zhong W, Cai Z (2007) Long-term effects of inorganic fertilizers on microbial biomass and community functional diversity in a paddy soil derived from quaternary red clay. Appl Soil Ecol 36:84–91