Application of compost and clay under water-stressed conditions influences functional diversity of rhizosphere bacteria

  • Bede S. Mickan
  • Lynette K. Abbott
  • Jingwei Fan
  • Miranda M. Hart
  • Kadambot H. M. Siddique
  • Zakaria M. Solaiman
  • Sasha N. Jenkins
Original Paper

Abstract

Applications of compost and clay to ameliorate soil constraints such as water stress are potential management strategies for sandy agricultural soils. Water repellent sandy soils in rain-fed agricultural systems limit production and have negative environmental effects associated with leaching and soil erosion. The aim was to determine whether compost and clay amendments in a sandy agricultural soil influenced the rhizosphere microbiome of Trifolium subterraneum under differing water regimes. Soil was amended with compost (2% w/w), clay (5% w/w) and a combination of both, in a glasshouse experiment with well-watered and water-stressed (70 and 35% field capacity) treatments. Ion Torrent 16S rRNA sequencing and Phylogenetic Investigation of Communities by Reconstruction of Unobserved States (PICRUSt) analysis of functional gene prediction were used to characterise the rhizosphere bacterial community and its functional component involved in nitrogen (N) cycling and soil carbon (C) degradation. Compost soil treatments increased the relative abundance of copiotrophic bacteria, decreased labile C and increased the abundance of recalcitrant C degrading genes. Predicted N cycling genes increased with the addition of clay (N2 fixation, nitrification, denitrification) and compost + clay (N2 fixation, denitrification) and decreased with compost (for denitrification) amendment. Water stress did not alter the relative abundance of phylum level taxa in the presence of compost, although copiotrophic Actinobacteria increased in relative abundance with addition of clay and with compost + clay. A significant role of compost and clay under water stress in influencing the composition of rhizosphere bacteria and their implications for N cycling and C degradation was demonstrated.

Keywords

Rhizosphere bacterial gene frequency PICRUSt Water stress Arbuscular mycorrhiza 

Supplementary material

374_2017_1238_MOESM1_ESM.doc (34 kb)
ESM 1(DOC 34 kb)
374_2017_1238_MOESM2_ESM.png (101 kb)
Supplementary Fig. S1Rarefaction curve for (a) well-watered treatment (35% FC), (b) water-stressed treatment (70% FC). Soil treatments are the addition of compost (2% w/w), clay (5% w/w) and the combination of compost and clay (2% w/w, 5% w/w) respectively. Error bars are the standard error of the mean (n = 4). (PNG 100 kb)
374_2017_1238_MOESM3_ESM.png (73 kb)
Supplementary Fig. S2Relative abundance of the rhizosphere bacteria (phylum) community for (top) water-stressed (35% FC) and (b) well-watered conditions (70% FC) from the addition of compost (2% w/w), clay (5% w/w) and the combination of compost and clay (2% w/w, 5% w/w) respectively. Error bars are the standard error of the mean (n = 4). (PNG 72 kb)
374_2017_1238_MOESM4_ESM.png (40 kb)
Supplementary Fig. S3Gene count of detected Nitrogen cycling genes under different soil treatments. Soil treatments are the addition of compost (2% w/w), clay (5% w/w) and the combination of compost and clay (2% w/w, 5% w/w) respectively (control is no addition of compost or clay). The bars represent the mean for each treatment and the error bars are the standard error of the mean (n = 4). (PNG 39 kb)
374_2017_1238_MOESM5_ESM.png (45 kb)
Supplementary Fig. S4Gene count of detected C degrading genes under different soil treatments. Soil treatments are the addition of compost (2% w/w), clay (5% w/w) and the combination of compost and clay (2% w/w, 5% w/w) respectively (control is no addition of compost or clay). The complexity of the C substrates is presented in order from labile (starch) to recalcitrant (lignin). The bars represent the mean for each treatment and the error bars are the standard error of the mean (n = 4). (PNG 44 kb)

References

  1. Abbott LK, Robson AD (1981) Infectivity and effectiveness of vesicular arbuscular mycorrhizal fungi: effect of inoculum type. Aus J Agri Res 32:631–639CrossRefGoogle Scholar
  2. Achouak W, Normand P, Heulin T (1999) Comparative phylogeny of rrs and nifH genes in the Bacillaceae. Inter J Syst Bacteriol 49:961–967CrossRefGoogle Scholar
  3. Anand RR, Paine M (2002) Regolith geology of the Yilgarn Craton, Western Australia: implications for exploration. Aus J Earth Sci 49:3–162CrossRefGoogle Scholar
  4. Baldock JA, Skjemstad JO (2000) Role of the soil matrix and minerals in protecting natural organic materials against biological attack. Org Geochem 31:697–710CrossRefGoogle Scholar
  5. Bar-Tal A, Yermiyahu U, Beraud J, Keinan M, Rosenberg R, Zohar D, Rosen V, Fine P (2004) Nitrogen, phosphorus, and potassium uptake by wheat and their distribution in soil following successive annual compost applications. J Env Qual 33:1855–1865CrossRefGoogle Scholar
  6. Barton L, Gleeson DB, Maccarone LD, Zúñiga LP, Murphy DV (2013) Is liming soil a strategy for mitigating nitrous oxide emissions from semi-arid soils? Soil Biol Biochem 62:28–35CrossRefGoogle Scholar
  7. Barzegar AR, Yousefi A, Daryashenas A (2002) The effect of addition of different amounts and types of organic materials on soil physical properties and yield of wheat. Plant Soil 247:295–301CrossRefGoogle Scholar
  8. Betti G, Grant C, Churchman G, Murray R (2015) Increased profile wettability in texture-contrast soils from clay delving: case studies in South Australia. Soil Res 53:125–136Google Scholar
  9. Blagodatskaya EV, Blagodatsky SA, Anderson TH, Kuzyakov Y (2007) Priming effects in Chernozem induced by glucose and N in relation to microbial growth strategies. Appl Soil Ecol 37:95–105CrossRefGoogle Scholar
  10. Blagodatskaya EV, Blagodatsky SA, Anderson TH, Kuzyakov Y (2014) Microbial growth and carbon use efficiency in the rhizosphere and root-free soil. PLoS One 9(4)Google Scholar
  11. Blakemore LC, Searle PL, Daly BK (1972) Methods for chemical analysis of soils. NZ Soil Bureau Scientific Report 10AGoogle Scholar
  12. Bowles TM, Acosta-Martínez V, Calderón F, Jackson LE (2014) soil enzyme activities, microbial communities, and carbon and nitrogen availability in organic agroecosystems across an intensively-managed agricultural landscape. Soil Biol Biochem 68:252–262CrossRefGoogle Scholar
  13. Bremner JM, Mulvaney CS (1982) Nitrogen total. Methods of soil analysis, part 2. American Soc Agro and Soil Sci Soc America, Madison, pp. 595–624Google Scholar
  14. Bronick CJ, Lal R (2005) Soil structure and management: a review. Geoderma 124:3–22CrossRefGoogle Scholar
  15. Cavagnaro TR (2014) Impacts of compost application on the formation and functioning of arbuscular mycorrhizas. Soil Biol Biochem 78:38–44CrossRefGoogle Scholar
  16. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Tumbaug PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336CrossRefPubMedPubMedCentralGoogle Scholar
  17. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME 6:1621–1624CrossRefGoogle Scholar
  18. Carvalho M, Brito I, Alho L, Goss MJ (2015) Assessing the progress of colonization by plant species under different temperature regimes. J Plant Nutr Soil Sci 178:515–522CrossRefGoogle Scholar
  19. Chen YP, Chen GS, Robinson D, Yang ZJ, Guo JF, Xie JS, Fu SL, Zhou LX, Yang YS (2016a) Large amounts of easily decomposable carbon stored in subtropical forest subsoil are associated with r-strategy-dominated soil microbes. Soil Biol Biochem 95:233–242CrossRefGoogle Scholar
  20. Chen Y, Chen G, Robinson D, Yang Z, Guo J, Xie J, Yang Y (2016b) Large amounts of easily decomposable carbon stored in subtropical forest subsoil is associated with r-strategy-dominated soil microbes. Soil Biol Biochem 95:233–242CrossRefGoogle Scholar
  21. Chowdhury SP, Schmid M, Hartmann A, Tripathi AK (2009) Diversity of 16S-rRNA and nifH genes derived from rhizosphere soil and roots of an endemic drought tolerant grass, Lasiurus sindicus. Euro J Soil Biol 45:114–122CrossRefGoogle Scholar
  22. Chaudhry V, Rehman A, Mishra A, Chauhan PS, Nautiyal CS (2012) Changes in bacterial community structure of agricultural land due to long-term organic and chemical amendments. Microbial Ecol 64:450–460CrossRefGoogle Scholar
  23. Cozzolino V, Di Meo V, Monda H, Spaccini R, Piccolo A (2016) The molecular characteristics of compost affect plant growth, arbuscular mycorrhizal fungi, and soil microbial community composition. Biol Fert Soils 52:15–29CrossRefGoogle Scholar
  24. Djajadi ALK, Hinz C (2012) Synergistic impacts of clay and organic matter on structural and biological properties of a sandy soil. Geoderma 183:19–24CrossRefGoogle Scholar
  25. Drury CF, Reynolds WD, Yang XM, Tan CS, Guo X, McKenney DJ, Fleming R, Denholme K (2014) Influence of compost source on corn grain yields, nitrous oxide and carbon dioxide emissions in southwestern Ontario. Can J Soil Sci 94:347–355CrossRefGoogle Scholar
  26. DeVries FT, Shade A (2013) Controls on soil microbial community stability under climate change. Front Microbiol 4:265Google Scholar
  27. Duong TT, Penfold C, Marschner P (2012) Amending soils of different texture with six compost types: impact on soil nutrient availability, plant growth and nutrient uptake. Plant Soil 354:197–209CrossRefGoogle Scholar
  28. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200CrossRefPubMedPubMedCentralGoogle Scholar
  29. Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364CrossRefPubMedGoogle Scholar
  30. Fuchslueger L, Bahn M, Fritz K, Hasibeder R, Richter A (2014) Experimental drought reduces the transfer of recently fixed plant carbon to soil microbes and alters the bacterial community composition in a mountain meadow. New Phytol 201:916–927CrossRefPubMedGoogle Scholar
  31. Fontaine S, Mariotti A, Abbadie L (2003) The priming effect of organic matter: a question of microbial competition? Soil Biol Biochem 35:837–843CrossRefGoogle Scholar
  32. Galbally IE, Kirstine WV, Meyer CP, Wang YP (2008) Soil–atmosphere trace gas exchange in semiarid and arid zones. J Environ Quality 37:599–607CrossRefGoogle Scholar
  33. Gihring TM, Green SJ, Schadt CW (2011) Massively parallel rRNA gene sequencing exacerbates the potential for biased community diversity comparisons due to variable library sizes. Environ Microbiol 14:285–290CrossRefPubMedGoogle Scholar
  34. Giles ME, Morley NJ, Baggs EM, Daniell TJ (2012) Soil nitrate reducing processes—drivers, mechanisms for spatial variation, and significance for nitrous oxide production. Front Microbiol 3:407CrossRefPubMedPubMedCentralGoogle Scholar
  35. Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500CrossRefGoogle Scholar
  36. Gleeson D, Mathes F, Farrell M, Leopold M (2016) Environmental drivers of soil microbial community structure and function at the Avon River Critical Zone Observatory. Sci Total Environ 571:1407–1418CrossRefPubMedGoogle Scholar
  37. Goodfellow M, Williams ST (1983) Ecology of actinomycetes. Ann Rev Microbiol 37:189–216CrossRefGoogle Scholar
  38. Gu J, Nicoullaud B, Rochette P, Grossel A, Henault C, Cellier P, Richard G (2013) A regional experiment suggests that soil texture is a major control of N2O emissions from tile-drained winter wheat fields during the fertilization period. Soil Biol Biochem 60:134–141CrossRefGoogle Scholar
  39. Guldimann C, Boor KJ, Wiedmann M, Guariglia-Oropeza V (2016) Resilience in the face of uncertainty: sigma factor B fine-tunes gene expression to support homeostasis in gram-positive bacteria. Appl Environ Microbiol 82:4456–4469CrossRefPubMedPubMedCentralGoogle Scholar
  40. Gupta V, Roper MM (2010) Protection of free-living nitrogen-fixing bacteria within the soil matrix. Soil Till Res 109:50–54CrossRefGoogle Scholar
  41. Hall DJM, Jones HR, Crabtree WL, Daniels ZL (2010) Claying and deep ripping can increase crop yields and profits on water repellent sands with marginal fertility in southern Western Australia. Soil Res 48:178–187CrossRefGoogle Scholar
  42. Hernández T, Garcia E, García C (2015) A strategy for marginal semiarid degraded soil restoration: a sole addition of compost at a high rate. A five-year field experiment. Soil Biol Biochem 89:61–71CrossRefGoogle Scholar
  43. Hoyle FC, D’Antuono M, Overheu T, Murphy DV (2013) Capacity for increasing soil organic carbon stocks in dryland agricultural systems. Soil Res 51:657–667CrossRefGoogle Scholar
  44. Ihaka R, Gentleman R (1996) R: a language for data analysis and graphics. J Comput Graph Stat 5:299–314Google Scholar
  45. IPCC (2007) Climate change 2007: impacts, adaption and vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USAGoogle Scholar
  46. Islam MR, Trivedi P, Palaniappan P, Reddy MS, Sa T (2009) Evaluating the effect of fertilizer application on soil microbial community structure in rice based cropping system using fatty acid methyl esters (FAME) analysis. World J Microbiol Biotechnol 25:1115–1117CrossRefGoogle Scholar
  47. Jenkins SN, Rushton SP, Lanyon CV, Whiteley AS, Waite IS, Brookes PC, Kemmitt S, Evershed RP, O’Donnell AG (2010) Taxon-specific responses of soil bacteria to the addition of low level C inputs. Soil Biol Biochem 42:1624–1631CrossRefGoogle Scholar
  48. Jenkins SN, Murphy DV, Waite IS, Rushton SP, O’Donnell AG (2016) Ancient landscapes and the relationship with microbial nitrification. Sci Rep 6:30733CrossRefPubMedPubMedCentralGoogle Scholar
  49. Jenkins SN, Waite IS, Blackburn A, Husband R, Rushton SP, Manning DC, O'Donnell AG (2009) Actinobacterial community dynamics in long term managed grasslands. Antonie Van Leeuwenhoek Inter J Gen Mol Microbiol 95:319–334CrossRefGoogle Scholar
  50. Kempers AJ, Luft AG (1988) Re-examination of the determination of environmental nitrate as nitrite by reduction with hydrazine. Analyst 113:1117–1120CrossRefPubMedGoogle Scholar
  51. Khalil MI, Hossain MB, Schmidhalter U (2005) Carbon and nitrogen mineralization in different upland soils of the subtropics treated with organic materials. Soil Biol Biochem 37:1507–1518CrossRefGoogle Scholar
  52. Koller R, Rodriguez A, Robin C, Scheu S, Bonkowski M (2013) Protozoa enhance foraging efficiency of arbuscular mycorrhizal fungi for mineral nitrogen from organic matter in soil to the benefit of host plants. New Phytol 199:203–211CrossRefPubMedGoogle Scholar
  53. Krull ES, Baldock JA, Skjemstad JO (2003) Importance of mechanisms and processes of the stabilisation of soil organic matter for modelling carbon turnover. Funct Plant Biol 30:207–222CrossRefGoogle Scholar
  54. Langenheder S, Prosser JI (2008) Resource availability influences the diversity of a functional group of heterotrophic soil bacteria. Environ Microbiol 10:2245–2256CrossRefPubMedGoogle Scholar
  55. Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Thurber RLV, Knight R, Beiko RG (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nature Biotechnol 31:814–821CrossRefGoogle Scholar
  56. Lavecchia A, Curci M, Jangid K, Whitman WB, Ricciuti P, Pascazio S, Crecchio C (2015) Microbial 16S gene-based composition of a sorghum cropped rhizosphere soil under different fertilization managements. Biol Fertil Soils 51:661–672CrossRefGoogle Scholar
  57. Lesaulnier C, Papamichail D, McCorkle S, Ollivier B, Skiena S, Taghavi S, Zak D, van der Lelie D (2008) Elevated atmospheric CO2 affects soil microbial diversity associated with trembling aspen. Environ Microbiol 10:926CrossRefPubMedGoogle Scholar
  58. Levy-Booth DJ, Prescott CE, Grayston SJ (2014) Microbial functional genes involved in nitrogen fixation, nitrification and denitrification in forest ecosystems. Soil Biol Biochem 75:11–25CrossRefGoogle Scholar
  59. Lützow MV, Kögel-Knabner I, Ekschmitt K, Matzner E, Guggenberger G, Marschner B, Flessa H (2006) Stabilization of organic matter in temperate soils: mechanisms and their relevance under different soil conditions—a review. Euro J Soil Sci 57:426–445CrossRefGoogle Scholar
  60. Manzoni S, Schimel JP, Porporato A (2012) Responses of soil microbial communities to water stress: results from a meta-analysis. Ecology 93:930–938CrossRefPubMedGoogle Scholar
  61. McDonald RIR, Speight J, Walker J, Hopkins M (1998) Australian soil and land survey field handbook. CSIRO Publishing, CanberraGoogle Scholar
  62. Metcalf JL, Xu ZZ, Weiss S, Lax S, Van Treuren W, Hyde ER, Song SJ, Amir A, Larsen P, Sangwan N, Haarmann D (2016) Microbial community assembly and metabolic function during mammalian corpse decomposition. Science 351(6269):158–162CrossRefPubMedGoogle Scholar
  63. Mickan BS, Abbott LK, Stefanova K, Solaiman ZM (2016) Interactions between biochar and mycorrhizal fungi in a water-stressed agricultural soil. Mycorrhiza 16:565–574CrossRefGoogle Scholar
  64. Mori H, Maruyama F, Kato H, Toyoda A, Dozono A, Ohtsubo Y, Nagata Y, Fujiyama A, Tsuda M, Kurokawa K (2013) Design and experimental application of a novel non-degenerate universal primer set that amplifies prokaryotic 16S rRNA genes with a low possibility to amplify eukaryotic rRNA genes. DNA Res 21:217–227CrossRefPubMedPubMedCentralGoogle Scholar
  65. Müller K, Deurer M (2011) Review of the remediation strategies for soil water repellency. Agric Ecosystems Environ 144:208–221CrossRefGoogle Scholar
  66. Ng EL, Patti AF, Rose MT, Schefe CR, Smernik RJ, Cavagnaro TR (2015) Do organic inputs alter resistance and resilience of soil microbial community to drying? Soil Biol Biochem 81:58–66CrossRefGoogle Scholar
  67. Ng EL, Patti AF, Rose MT, Schefe CR, Wilkinson K, Smernik RJ, Cavagnaro TR (2014) Does the chemical nature of soil carbon drive the structure and functioning of soil microbial communities? Soil Biol Biochem 70:54–61CrossRefGoogle Scholar
  68. Nulsen RA (1993) Changes in soil properties. In: Hobbs RJ, Saunders DA (eds) Reintegrating fragmented landscaped-towards sustainable production and nature conservation. Springer, New York, pp 107–145CrossRefGoogle Scholar
  69. Oades JM (1988) The retention of organic matter in soils. Biogeochemistry 5:35–70CrossRefGoogle Scholar
  70. Paranychianakis NV, Tsiknia M, Giannakis G, Nikolaidis NP, Kalogerakis N (2013) Nitrogen cycling and relationships between ammonia oxidizers and denitrifiers in a clay-loam soil. Applied Microbiol Biotechnol 97:5507–5515CrossRefGoogle Scholar
  71. Parkin TB (1987) Soil microsites as a source of denitrification variability. Soil Sci Soc Am J 5:1194–1199CrossRefGoogle Scholar
  72. Peacock AG, Mullen MD, Ringelberg DB, Tyler DD, Hedrick DB, Gale PM, White DC (2001) Soil microbial community responses to dairy manure or ammonium nitrate applications. Soil Biol Biochem 33:1011–1019CrossRefGoogle Scholar
  73. Pera A, Vallini G, Sireno I, Bianchin ML, De Bertoldi M (1983) Effect of organic matter on rhizosphere microorganisms and root development of sorghum plants in two different soils. Plant Soil 74:3–18CrossRefGoogle Scholar
  74. Pereira e Silva MC, Semenov AV, van Elsas JD, Salles JF (2011) Seasonal variations in the diversity and abundance of diazotrophic communities across soils. FEMS Microbiol Ecol 77:57–68CrossRefPubMedGoogle Scholar
  75. Pii Y, Borruso L, Brusetti L, Crecchio C, Cesco S, Mimmo T (2016) The interaction between iron nutrition, plant species and soil type shapes the rhizosphere microbiome. Plant Phys Biochem 99:39–48CrossRefGoogle Scholar
  76. Pii Y, Mimmo T, Tomasi N, Terzano R, Cesco S, Crecchio C (2015) Microbial interactions in the rhizosphere: beneficial influences of plant growth-promoting rhizobacteria on nutrient acquisition process. A review. Biol Fertil Soils 51:403–415CrossRefGoogle Scholar
  77. Prescott LM, Harle JP, Klein DA (1996) Microbiology. WCB McGraw-Hill, Boston, MAGoogle Scholar
  78. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glöckner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196CrossRefPubMedPubMedCentralGoogle Scholar
  79. Quilty JR, Cattle SR (2011) Use and understanding of organic amendments in Australian agriculture: a review. Soil Res 49:1–26CrossRefGoogle Scholar
  80. Roper MM (2004) The isolation and characterisation of bacteria with the potential to degrade waxes that cause water repellency in sandy soils. Soil Res 42:427–434CrossRefGoogle Scholar
  81. Saison C, Degrange V, Oliver R, Millard P, Commeaux C, Montange D, Le Roux X (2006) Alteration and resilience of the soil microbial community following compost amendment: effects of compost level and compost-borne microbial community. Environ Microbiol 8:247–257CrossRefPubMedGoogle Scholar
  82. Sánchez-García M, Sánchez-Monedero MA, Roig A, López-Cano I, Moreno B, Benitez E, Cayuela ML (2016) Compost vs biochar amendment: a two-year field study evaluating soil C build-up and N dynamics in an organically managed olive crop. Plant Soil 401:1–14CrossRefGoogle Scholar
  83. Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88:1386–1394CrossRefPubMedGoogle Scholar
  84. 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 75:7537–7541CrossRefPubMedPubMedCentralGoogle Scholar
  85. Schloss PD, Gevers D, Westcott SL (2011) Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6:12Google Scholar
  86. Searle PL (1984) The Berthelot or indophenol reaction and its use in the analytical chemistry of nitrogen. Rev Anal 109:549–568CrossRefGoogle Scholar
  87. Six J, Feller C, Denef K, Ogle S, Sa JCDM, Albrecht A (2002) Soil organic matter, biota and aggregation in temperate and tropical soils—effects of no-tillage. Agronomie 22:755–775CrossRefGoogle Scholar
  88. Sonia MT, Hafedh B, Abdennaceur H, Ali G (2011) Studies on the ecology of actinomycetes in an agricultural soil amended with organic residues: II. Assessment of enzymatic activities of Actinomycetales isolates. World J Microbiol Biotechnol 27:2251–2259CrossRefGoogle Scholar
  89. Stockdale EA, Banning NC, Murphy DV (2013) Rhizosphere effects on functional stability of microbial communities in conventional and organic soils following elevated temperature treatment. Soil Biol Biochem 57:56–59CrossRefGoogle Scholar
  90. Tisdall JM, Oades J (1982) Organic matter and water-stable aggregates in soils. J Soil Science 33:141–163CrossRefGoogle Scholar
  91. Trivedi P, Delgado-Baquerizo M, Trivedi C, Hu H, Anderson IC, Jeffries TC, Zhou J, Singh BK (2016) Microbial regulation of the soil carbon cycle: evidence from gene–enzyme relationships. ISME. https://doi.org/10.1038/ismej.2016.6
  92. van der Heijden MGA, Bardgett RD, Van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310CrossRefPubMedGoogle Scholar
  93. Ward NL, Challacombe JF, Janssen PH, Henrissat B, Coutinho PM, Wu M, Xie G, Haft DH, Sait M, Badger J, Barabote RD (2009) Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils. Appl Environ Microbiol 75:2046–2056CrossRefPubMedPubMedCentralGoogle Scholar
  94. Wang WJ, Dalala RC, Moodya PW, Smith CJ (2003) Relationships of soil respiration to microbial biomass, substrate availability and clay content. Soil Biol Biochem 35:273–284CrossRefGoogle Scholar
  95. Weerasekara AW, Jenkins S, Abbott LK, Waite I, McGrath JW, Larma I, Eroglu E, O’Donnell A, Whiteley AS (2016) Microbial phylogenetic and functional responses within acidified wastewater communities exhibiting enhanced phosphate uptake. Bioresource Technol 220:55–61CrossRefGoogle Scholar
  96. Welsh A, Chee-Sanford JC, Connor LM, Loffler FE, Sanford RA (2014) Refined NrfA phylogeny improves PCR-based nrfA gene detection. Appl Environ Microbiol 80:2110–2119CrossRefPubMedPubMedCentralGoogle Scholar
  97. White JR, Nagarajan N, Pop M (2009) Statistical methods for detecting differentially abundant features in clinical metagenomic samples. PLoS Comput Biol 5(4)Google Scholar
  98. Whiteley AS, Jenkins S, Waite I, Kresoje N, Payne H, Mullan B, Allcock R, O'Donnell A (2012) Microbial 16S rRNA Ion Tag and community metagenome sequencing using the Ion Torrent (PGM) Platform. J Microbiol Methods 91:80–88CrossRefPubMedGoogle Scholar
  99. Yoon S, Cruz-García C, Sanford R, Ritalahti KM, Löffler FE (2015) Denitrification versus respiratory ammonification: environmental controls of two competing dissimilatory NO3 /NO2 reduction pathways in Shewanella loihica strain PV-4. ISME 9:1093–1104CrossRefGoogle Scholar
  100. Zhu B, Gutknecht JL, Herman DJ, Keck DC, Firestone MK, Cheng W (2014) Rhizosphere priming effects on soil carbon and nitrogen mineralization. Soil Biol Biochem 76:183–192CrossRefGoogle Scholar
  101. Zhen Z, Liu H, Wang N, Guo L, Meng J, Ding N, Wu G, Jiang G (2014) Effects of manure compost application on soil microbial community diversity and soil microenvironments in a temperate cropland in China. PLoS One 9(10)Google Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Bede S. Mickan
    • 1
    • 2
    • 3
  • Lynette K. Abbott
    • 1
    • 2
  • Jingwei Fan
    • 4
  • Miranda M. Hart
    • 5
  • Kadambot H. M. Siddique
    • 1
    • 2
  • Zakaria M. Solaiman
    • 1
    • 2
  • Sasha N. Jenkins
    • 1
    • 2
  1. 1.UWA School of Agriculture and Environment (M079)The University of Western AustraliaPerthAustralia
  2. 2.The UWA Institute of Agriculture (M082)The University of Western AustraliaPerthAustralia
  3. 3.Richgro Garden ProductsJandakotAustralia
  4. 4.State Key Laboratory of Grassland Agro-ecosystems, Institute of Arid Agroecology, School of Life SciencesLanzhou UniversityLanzhouChina
  5. 5.BiologyUniversity of British Columbia OkanaganKelownaCanada

Personalised recommendations