Advertisement

Microbial Ecology

, Volume 78, Issue 3, pp 737–752 | Cite as

Biosolids and Tillage Practices Influence Soil Bacterial Communities in Dryland Wheat

  • Daniel C. Schlatter
  • Narayan C. Paul
  • Devendra H. Shah
  • William F. Schillinger
  • Andy I. Bary
  • Brenton Sharratt
  • Timothy C. PaulitzEmail author
Soil Microbiology

Abstract

Class B biosolids are used in dryland wheat (Triticum aestivum L.) production in eastern Washington as a source of nutrients and to increase soil organic matter, but little is known about their effects on bacterial communities and potential for harboring human pathogens. Moreover, conservation tillage is promoted to reduce erosion and soil degradation. We explored the impacts of biosolids or synthetic fertilizer in combination with traditional (conventional) or conservation tillage on soil bacterial communities. Bacterial communities were characterized from fresh biosolids, biosolid aggregates embedded in soil, and soil after a second application of biosolids using high-throughput amplicon sequencing. Biosolid application significantly affected bacterial communities, even 4 years after their application. Bacteria in the families Clostridiaceae, Norcardiaceae, Anaerolinaceae, Dietziaceae, and Planococcaceae were more abundant in fresh biosolids, biosolid aggregates, and soils treated with biosolids than in synthetically fertilized soils. Taxa identified as Turcibacter, Dietzia, Clostridiaceae, and Anaerolineaceae were highly abundant in biosolid aggregates in the soil and likely originated from the biosolids. In contrast, Oxalobacteriaceae, Streptomyceteaceae, Janthinobacterium, Pseudomonas, Kribbella, and Bacillus were rare in the fresh biosolids, but relatively abundant in biosolid aggregates in the soil, and probably originated from the soil to colonize the substrate. However, tillage had relatively minor effects on bacterial communities, with only a small number of taxa differing in relative abundance between traditional and conventional tillage. Although biosolid-associated bacteria persisted in soil, potentially pathogenic taxa were extremely rare and no toxin genes for key groups (Salmonella, Clostridium) were detectable, suggesting that although fecal contamination was apparent via indicator taxa, pathogen populations had declined to low levels. Thus, biosolid amendments had profound effects on soil bacterial communities both by introducing gut- or digester-derived bacteria and by enriching potentially beneficial indigenous soil populations.

Keywords

Biosolids Soil Microbiome Pathogens Tillage Wheat Dryland cropping systems 

Notes

Acknowledgements

The authors thank John Jacobsen and Bruce Sauer for their excellent assistance in the field management of this experiment.

Funding

Funding for the research was provided by the USDA-Agricultural Research Service, Washington State University, King County, Washington Department of Natural Resources, and Northwest Biosolids. D.C.S. was funded by an administrator-funded USDA-ARS Postdoctoral Research Associate Award.

Supplementary material

248_2019_1339_Fig9_ESM.jpg (244 kb)
Supplemental Figure 1 The biosolids experiment at Lind, WA was laid out in a split-block design to facilitate the application of biosolids with a manure spreader. There were two sets of plots so that both the winter wheat and fallow phases in the 2-year winter wheat-fallow rotation were present every year. Green represents the biosolid treatment and blue the synthetic fertilizer treatment. 1 = undercutter, 2 = disk. B = biosolid, S = synthetic. (JPG 243 kb)
248_2019_1339_Fig10_ESM.png (86 kb)
Supplemental Figure 2

Differentially abundant OTUs for tillage. Graph on left- both taxa are more abundant in conservation than traditional tillage in biosolid treatments. Graph on right- both taxa are more abundant in conservation than traditional tillage in synthetic fertilizer treatments. (PNG 85 kb)

248_2019_1339_MOESM1_ESM.tiff (256 kb)
High resolution image (TIFF 256 kb)

References

  1. 1.
    Crosson P (1995) Soil erosion estimates and costs. Science 269:461–464.  https://doi.org/10.1126/science.269.5223.461 CrossRefGoogle Scholar
  2. 2.
    Montgomery DR (2007) Soil erosion and agricultural sustainability. Proc Natl Acad Sci 104:13268–13272.  https://doi.org/10.1073/pnas.0611508104 CrossRefGoogle Scholar
  3. 3.
    Pimentel D, Harvey C, Resosudarmo P, Sinclair K, Kurz D, McNair M, Crist S, Shpritz L, Fitton L, Saffouri R, Blair R (1995) Environmental and economic costs of soil erosion and conservation benefits. Science 267:1117–1123.  https://doi.org/10.1126/science.267.5201.1117 CrossRefGoogle Scholar
  4. 4.
    Uri ND, Lewis JA (1999) Agriculture and the dynamics of soil erosion in the United States. J Sustain Agric 14:63–82.  https://doi.org/10.1300/J064v14n02_07 CrossRefGoogle Scholar
  5. 5.
    Singh P, Sharratt B, Schillinger WF (2012) Wind erosion and PM10 emission affected by tillage systems in the world’s driest rainfed wheat region. Soil Tillage Res 124:219–225.  https://doi.org/10.1016/j.still.2012.06.009 CrossRefGoogle Scholar
  6. 6.
    Sharratt B, Feng G, Wendling L (2007) Loss of soil and PM10 from agricultural fields associated with high winds on the Columbia Plateau. Earth Surf Process Landf 32:621–630.  https://doi.org/10.1002/esp.1425 CrossRefGoogle Scholar
  7. 7.
    Schillinger WF, Young DL (2004) Cropping systems research in the world’s driest rainfed wheat region. Agron J 96:1182.  https://doi.org/10.2134/agronj2004.1182 CrossRefGoogle Scholar
  8. 8.
    Schlatter DC, Schillinger WF, Bary AI, Sharratt B, Paulitz TC (2017) Biosolids and conservation tillage: impacts on soil fungal communities in dryland wheat-fallow cropping systems. Soil Biol Biochem 115:556–567.  https://doi.org/10.1016/j.soilbio.2017.09.021 CrossRefGoogle Scholar
  9. 9.
    Wade T, Claassen R, Wallander S (2015) Conservation-tillage practice adoption rates vary widely by crop and region. USDA-ARS Econ Inf Bull 147Google Scholar
  10. 10.
    Lal R, Reicosky DC, Hanson JD (2007) Evolution of the plow over 10,000 years and the rationale for no-till farming. Soil Tillage Res 93:1–12.  https://doi.org/10.1016/j.still.2006.11.004 CrossRefGoogle Scholar
  11. 11.
    Young I, Ritz K (2000) Tillage, habitat space and function of soil microbes. Soil Tillage Res 53:201–213.  https://doi.org/10.1016/S0167-1987(99)00106-3 CrossRefGoogle Scholar
  12. 12.
    Govaerts B, Mezzalama M, Unno Y, Sayre KD, Luna-Guido M, Vanherck K, Dendooven L, Deckers J (2007) Influence of tillage, residue management, and crop rotation on soil microbial biomass and catabolic diversity. Appl Soil Ecol 37:18–30.  https://doi.org/10.1016/j.apsoil.2007.03.006 CrossRefGoogle Scholar
  13. 13.
    Yin C, Mueth N, Hulbert S, Schlatter D, Paulitz TC, Schroeder K, Prescott A, Dhingra A (2017) Bacterial communities on wheat grown under long-term conventional tillage and no-till in the Pacific Northwest of the United States. Phytobiomes 1:83–90.  https://doi.org/10.1094/PBIOMES-09-16-0008-R CrossRefGoogle Scholar
  14. 14.
    Wuest SB, Schillinger WF (2011) Evaporation from high residue no-till versus tilled fallow in a dry summer climate. Soil Sci Soc Am J 75:1513.  https://doi.org/10.2136/sssaj2010.0368 CrossRefGoogle Scholar
  15. 15.
    Young DL, Schillinger WF (2012) Wheat farmers adopt the undercutter fallow method to reduce wind erosion and sustain profitability. Soil Tillage Res 124:240–244.  https://doi.org/10.1016/j.still.2012.07.001 CrossRefGoogle Scholar
  16. 16.
    Diacono M, Montemurro F (2010) Long-term effects of organic amendments on soil fertility. A review. Agron Sustain Dev 30:401–422.  https://doi.org/10.1051/agro/2009040 CrossRefGoogle Scholar
  17. 17.
    Lu Q, He ZL, Stoffella PJ (2012) Land application of biosolids in the USA: a review. Appl Environ Soil Sci 2012:1–11.  https://doi.org/10.1155/2012/201462 CrossRefGoogle Scholar
  18. 18.
    Rigby H, Clarke BO, Pritchard DL, Meehan B, Beshah F, Smith SR, Porter NA (2016) A critical review of nitrogen mineralization in biosolids-amended soil, the associated fertilizer value for crop production and potential for emissions to the environment. Sci Total Environ 541:1310–1338.  https://doi.org/10.1016/j.scitotenv.2015.08.089 CrossRefGoogle Scholar
  19. 19.
    Wuest SB, Gollany HT (2013) Soil organic carbon and nitrogen after application of nine organic amendments. Soil Sci Soc Am J 77:237.  https://doi.org/10.2136/sssaj2012.0184 CrossRefGoogle Scholar
  20. 20.
    Wallace BM, Krzic M, Forge TA, Broersma K, Newman RF (2009) Biosolids increase soil aggregation and protection of soil carbon five years after application on a crested wheatgrass pasture. J Environ Qual 38:291.  https://doi.org/10.2134/jeq2007.0608 CrossRefGoogle Scholar
  21. 21.
    García-Orenes F, Guerrero C, Mataix-Solera J, Navarro-Pedreño J, Gómez I, Mataix-Beneyto J (2005) Factors controlling the aggregate stability and bulk density in two different degraded soils amended with biosolids. Soil Tillage Res 82:65–76.  https://doi.org/10.1016/j.still.2004.06.004 CrossRefGoogle Scholar
  22. 22.
    Pi H, Sharratt B, Schillinger WF, Bary AI, Cogger CG (2018) Wind erosion potential of a winter wheat–summer fallow rotation after land application of biosolids. Aeolian Res 32:53–59.  https://doi.org/10.1016/j.aeolia.2018.01.009 CrossRefGoogle Scholar
  23. 23.
    Pepper IL, Zerzghi H, Brooks JP, Gerba CP (2008) Sustainability of land application of Class B biosolids. J Environ Qual 37:S-58.  https://doi.org/10.2134/jeq2007.0321 CrossRefGoogle Scholar
  24. 24.
    Zerzghi H, Gerba CP, Brooks JP, Pepper IL (2010) Long-term effects of land application of class B biosolids on the soil microbial populations, pathogens, and activity. J Environ Qual 39:402.  https://doi.org/10.2134/jeq2009.0307 CrossRefGoogle Scholar
  25. 25.
    Gerba CP, Smith JE (2005) Sources of pathogenic microorganisms and their fate during land application of wastes. J Environ Qual 34:42–48Google Scholar
  26. 26.
    Fijalkowski K, Rorat A, Grobelak A, Kacprzak MJ (2017) The presence of contaminations in sewage sludge—the current situation. J Environ Manag 203:1126–1136.  https://doi.org/10.1016/j.jenvman.2017.05.068 CrossRefGoogle Scholar
  27. 27.
    Lang NL, Smith SR (2007) Influence of soil type, moisture content and biosolids application on the fate of Escherichia coli in agricultural soil under controlled laboratory conditions: E. coli decay in sludge-amended soil. J Appl Microbiol 103:2122–2131.  https://doi.org/10.1111/j.1365-2672.2007.03490.x CrossRefGoogle Scholar
  28. 28.
    Chandler D, Craven J (1980) Relationship of soil moisture to survival of Escherichia coli and Salmonella typhimurium in soils. Aust J Agric Res 31:547.  https://doi.org/10.1071/AR9800547 CrossRefGoogle Scholar
  29. 29.
    Gibbs R, Hu C, Ho G, Unkovich I (1997) Regrowth of faecal coliforms and salmonellae in stored biosolids and soil amended with biosolids. Water Sci Technol 35.  https://doi.org/10.1016/S0273-1223(97)00271-0
  30. 30.
    Zhou J, He Z, Yang Y, et al (2015) High-throughput metagenomic technologies for complex microbial community analysis: open and closed formats. mBio 6.  https://doi.org/10.1128/mBio.02288-14
  31. 31.
    Bibby K, Viau E, Peccia J (2010) Pyrosequencing of the 16S rRNA gene to reveal bacterial pathogen diversity in biosolids. Water Res 44:4252–4260.  https://doi.org/10.1016/j.watres.2010.05.039 CrossRefGoogle Scholar
  32. 32.
    Federer WT, King F (2007) Variations on split plot and split block experiment designs. John Wiley & Sons, Inc., Hoboken, NJCrossRefGoogle Scholar
  33. 33.
    Pi H, Sharratt B, Schillinger WF, Bary A, Cogger C (2018) Chemical composition of windblown dust emitted from agricultural soils amended with biosolids. Aeolian Res 32:102–115.  https://doi.org/10.1016/j.aeolia.2018.02.001 CrossRefGoogle Scholar
  34. 34.
    Gohl DM, Vangay P, Garbe J, MacLean A, Hauge A, Becker A, Gould TJ, Clayton JB, Johnson TJ, Hunter R, Knights D, Beckman KB (2016) Systematic improvement of amplicon marker gene methods for increased accuracy in microbiome studies. Nat Biotechnol 34:942–949.  https://doi.org/10.1038/nbt.3601 CrossRefGoogle Scholar
  35. 35.
    Zhang J, Kobert K, Flouri T, Stamatakis A (2014) PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics 30:614–620.  https://doi.org/10.1093/bioinformatics/btt593 CrossRefGoogle Scholar
  36. 36.
    Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnetjournal 17:10.  https://doi.org/10.14806/ej.17.1.200 Google Scholar
  37. 37.
    Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996–998.  https://doi.org/10.1038/nmeth.2604 CrossRefGoogle Scholar
  38. 38.
    Rognes, T., Flouri, T., Nichols B, et al (2016) VSEARCH: a versatile open source tool for metagenomics.  https://doi.org/10.7287/peerj.preprints.2409v1
  39. 39.
    Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267  https://doi.org/10.1128/AEM.00062-07 CrossRefGoogle Scholar
  40. 40.
    Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña 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, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336.  https://doi.org/10.1038/nmeth.f.303 CrossRefGoogle Scholar
  41. 41.
    Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15.  https://doi.org/10.1186/s13059-014-0550-8
  42. 42.
    Meer RR, Songer JG (1997) Multiplex polymerase chain reaction assay for genotyping Clostridium perfringens. Am J Vet Res 58:702–705Google Scholar
  43. 43.
    Gohari IM, Parreira VR, Nowell VJ, Nicholson VM, Oliphant K, Prescott JF (2015) A novel pore-forming toxin in type A Clostridium perfringens is associated with both fatal canine hemorrhagic gastroenteritis and fatal foal necrotizing enterocolitis. PLoS One 10:e0122684.  https://doi.org/10.1371/journal.pone.0122684 CrossRefGoogle Scholar
  44. 44.
    Rahn K, De Grandis SA, Clarke RC, McEwen SA, Galán JE, Ginocchio C, Curtiss R, Gyles CL (1992) Amplification of an invA gene sequence of Salmonella typhimurium by polymerase chain reaction as a specific method of detection of Salmonella. Mol Cell Probes 6(4):271–279CrossRefGoogle Scholar
  45. 45.
    Oksanen J, Blanchette FG, Friendly M, et al (2016) Vegan: Community ecology packageGoogle Scholar
  46. 46.
    Rubin BER, Gibbons SM, Kennedy S, Hampton-Marcell J, Owens S, Gilbert JA (2013) Investigating the impact of storage conditions on microbial community composition in soil samples. PLoS One 8:e70460.  https://doi.org/10.1371/journal.pone.0070460 CrossRefGoogle Scholar
  47. 47.
    Cogger CG, Bary AI, Myhre EA, Fortuna A-M (2013) Biosolids applications to tall fescue have long-term influence on soil nitrogen, carbon, and phosphorus. J Environ Qual 42:516.  https://doi.org/10.2134/jeq2012.0269 CrossRefGoogle Scholar
  48. 48.
    Mantovi P, Baldoni G, Toderi G (2005) Reuse of liquid, dewatered, and composted sewage sludge on agricultural land: effects of long-term application on soil and crop. Water Res 39:289–296.  https://doi.org/10.1016/j.watres.2004.10.003 CrossRefGoogle Scholar
  49. 49.
    Karpowicz E, Novinscak A, Bärlocher F, Filion M (2010) qPCR quantification and genetic characterization of Clostridium perfringens populations in biosolids composted for 2 years. J Appl Microbiol 108:571–581.  https://doi.org/10.1111/j.1365-2672.2009.04441.x CrossRefGoogle Scholar
  50. 50.
    Stefanis C, Alexopoulos A, Voidarou C, Vavias S, Bezirtzoglou E (2014) Prevalence of C. perfringens in agricultural fields with different vegetation types. Folia Microbiol (Praha) 59:1–4.  https://doi.org/10.1007/s12223-013-0257-3 CrossRefGoogle Scholar
  51. 51.
    Xu C, Wang D, Huber A, Weese SJ, Warriner K (2016) Persistence of Clostridium difficile in wastewater treatment-derived biosolids during land application or windrow composting. J Appl Microbiol 120:312–320.  https://doi.org/10.1111/jam.13018 CrossRefGoogle Scholar
  52. 52.
    Xu C, Weese JS, Flemming C, Odumeru J, Warriner K (2014) Fate of Clostridium difficile during wastewater treatment and incidence in Southern Ontario watersheds. J Appl Microbiol 117:891–904.  https://doi.org/10.1111/jam.12575 CrossRefGoogle Scholar
  53. 53.
    Sidhu J, Gibbs RA, Ho GE, Unkovich I (2001) The role of indigenous microorganisms in suppression of Salmonella regrowth in composted biosolids. Water Res 35:913–920CrossRefGoogle Scholar
  54. 54.
    Bonjoch X, Blanch AR (2009) Resistance of faecal coliforms and enterococci populations in sludge and biosolids to different hygienisation treatments. Microb Ecol 57:478–483.  https://doi.org/10.1007/s00248-008-9430-7 CrossRefGoogle Scholar
  55. 55.
    Zerzghi H, Brooks JP, Gerba CP, Pepper IL (2010) Influence of long-term land application of class B biosolids on soil bacterial diversity. J Appl Microbiol.  https://doi.org/10.1111/j.1365-2672.2010.04698.x
  56. 56.
    Rojo D, Méndez-García C, Raczkowska BA, Bargiela R, Moya A, Ferrer M, Barbas C (2017) Exploring the human microbiome from multiple perspectives: factors altering its composition and function. FEMS Microbiol Rev 41:453–478.  https://doi.org/10.1093/femsre/fuw046 CrossRefGoogle Scholar
  57. 57.
    Flemming CA, Simhon A, Odumeru JA (2017) Pathogen characterization of fresh and stored mesophilic anaerobically digested biosolids. Water Environ Res 89:2031–2042.  https://doi.org/10.2175/106143017X14839994522704 CrossRefGoogle Scholar
  58. 58.
    Yamada T (2006) Anaerolinea thermolimosa sp. nov., Levilinea saccharolytica gen. nov., sp. nov. and Leptolinea tardivitalis gen. nov., sp. nov., novel filamentous anaerobes, and description of the new classes Anaerolineae classis nov. and Caldilineae classis nov. in the bacterial phylum Chloroflexi. Int J Syst Evol Microbiol 56:1331–1340.  https://doi.org/10.1099/ijs.0.64169-0 CrossRefGoogle Scholar
  59. 59.
    Zhang B, Xu X, Zhu L (2017) Structure and function of the microbial consortia of activated sludge in typical municipal wastewater treatment plants in winter. Sci Rep 7.  https://doi.org/10.1038/s41598-017-17743-x
  60. 60.
    McIlroy SJ, Kirkegaard RH, Dueholm MS, et al (2017) Culture-independent analyses reveal novel Anaerolineaceae as abundant primary fermenters in anaerobic digesters treating waste activated sludge. Front Microbiol 8.  https://doi.org/10.3389/fmicb.2017.01134
  61. 61.
    Bosshard PP, Altwegg M, Zbinden R (2002) Turicibacter sanguinis gen. nov., sp. nov., a novel anaerobic, Gram-positive bacterium. Int J Syst Evol Microbiol 52:1263–1266.  https://doi.org/10.1099/00207713-52-4-1263 Google Scholar
  62. 62.
    Fan P, Liu P, Song P, Chen X, Ma X (2017) Moderate dietary protein restriction alters the composition of gut microbiota and improves ileal barrier function in adult pig model. Sci Rep 7:43412.  https://doi.org/10.1038/srep43412 CrossRefGoogle Scholar
  63. 63.
    Kim M, Kim J, Kuehn LA, Bono JL, Berry ED, Kalchayanand N, Freetly HC, Benson AK, Wells JE (2014) Investigation of bacterial diversity in the feces of cattle fed different diets1. J Anim Sci 92:683–694.  https://doi.org/10.2527/jas.2013-6841 CrossRefGoogle Scholar
  64. 64.
    Li D, Chen H, Mao B et al (2017) Microbial biogeography and core microbiota of the rat digestive tract. Sci Rep 8:45840.  https://doi.org/10.1038/srep45840 CrossRefGoogle Scholar
  65. 65.
    Pu S, Khazanehei H, Jones PJ, Khafipour E (2016) Interactions between obesity status and dietary intake of monounsaturated and polyunsaturated oils on human gut microbiome profiles in the Canola Oil Multicenter Intervention Trial (COMIT). Front Microbiol 7.  https://doi.org/10.3389/fmicb.2016.01612
  66. 66.
    Gharibzahedi SMT, Razavi SH, Mousavi M (2014) Potential applications and emerging trends of species of the genus Dietzia: a review. Ann Microbiol 64:421–429.  https://doi.org/10.1007/s13213-013-0699-5 CrossRefGoogle Scholar
  67. 67.
    Yamamura H, Lisdiyanti P, Ridwan R, Ratnakomala S, Sarawati R, Lestari Y, Triana E, Kartina G, Widyastuti Y, Ando K (2010) Dietzia timorensis sp. nov., isolated from soil. Int J Syst Evol Microbiol 60:451–454.  https://doi.org/10.1099/ijs.0.012229-0 CrossRefGoogle Scholar
  68. 68.
    Koerner RJ, Goodfellow M, Jones AL (2009) The genus Dietzia: a new home for some known and emerging opportunist pathogens. FEMS Immunol Med Microbiol 55:296–305.  https://doi.org/10.1111/j.1574-695X.2008.00513.x CrossRefGoogle Scholar
  69. 69.
    Gomez DE, Arroyo LG, Costa MC, Viel L, Weese JS (2017) Characterization of the fecal bacterial microbiota of healthy and diarrheic dairy calves. J Vet Intern Med 31:928–939.  https://doi.org/10.1111/jvim.14695 CrossRefGoogle Scholar
  70. 70.
    Blackall L, Harbers A, Greenfield P, Hayward A (1991) Foaming in activated sludge plants: a survey in Queensland, Australia and an evaluation of some control strategies. Water Res 25:313–317.  https://doi.org/10.1016/0043-1354(91)90011-E CrossRefGoogle Scholar
  71. 71.
    Blackall LL, Harbers AE, Greenfield PF, Hayward AC (1991) Activated sludge foams: effects of environmental variables on organism growth and foam formation. Environ Technol 12:241–248.  https://doi.org/10.1080/09593339109385001 CrossRefGoogle Scholar
  72. 72.
    Soddell JA, Seviour RJ (1995) Relationship between temperature and growth of organisms causing Nocardia foams in activated sludge plants. Water Res 29:1555–1558.  https://doi.org/10.1016/0043-1354(94)00222-S CrossRefGoogle Scholar
  73. 73.
    Derakhshani H, De Buck J, Mortier R, et al (2016) The features of fecal and ileal mucosa-associated microbiota in dairy calves during early infection with Mycobacterium avium subspecies paratuberculosis. Front Microbiol 7.  https://doi.org/10.3389/fmicb.2016.00426
  74. 74.
    Sohn K, Kalanetra KM, Mills DA, Underwood MA (2016) Buccal administration of human colostrum: impact on the oral microbiota of premature infants. J Perinatol 36:106–111.  https://doi.org/10.1038/jp.2015.157 CrossRefGoogle Scholar
  75. 75.
    Verma P, Yadav AN, Khannam KS, Kumar S, Saxena AK, Suman A (2016) Molecular diversity and multifarious plant growth promoting attributes of bacilli associated with wheat (Triticum aestivum L.) rhizosphere from six diverse agro-ecological zones of India: diversity and plant growth promoting attributes of bacilli. J Basic Microbiol 56:44–58.  https://doi.org/10.1002/jobm.201500459 CrossRefGoogle Scholar
  76. 76.
    Wang K, Zhang L, Li J, Pan Y, Meng L, Xu T, Zhang C, Liu H, Hong S, Huang H, Jiang J (2015) Planococcus dechangensis sp. nov., a moderately halophilic bacterium isolated from saline and alkaline soils in Dechang Township, Zhaodong City, China. Antonie Van Leeuwenhoek 107:1075–1083.  https://doi.org/10.1007/s10482-015-0399-1 CrossRefGoogle Scholar
  77. 77.
    Whitehead TR, Johnson CN, Patel NB, Cotta MA, Moore ERB, Lawson PA (2015) Savagea faecisuis gen. nov., sp. nov., a tylosin- and tetracycline-resistant bacterium isolated from a swine-manure storage pit. Antonie Van Leeuwenhoek 108:151–161.  https://doi.org/10.1007/s10482-015-0473-8 CrossRefGoogle Scholar
  78. 78.
    Baertsch C, Paez-Rubio T, Viau E, Peccia J (2007) Source tracking aerosols released from land-applied class B biosolids during high-wind events. Appl Environ Microbiol 73:4522–4531.  https://doi.org/10.1128/AEM.02387-06 CrossRefGoogle Scholar
  79. 79.
    Dowd SE, Widmer KW, Pillai SD (1997) Thermotolerant Clostridia as an airborne pathogen indicator during land application of biosolids. J Environ Qual 26:194.  https://doi.org/10.2134/jeq1997.00472425002600010028x CrossRefGoogle Scholar
  80. 80.
    Rouch DA, Mondal T, Pai S, Glauche F, Fleming VA, Thurbon N, Blackbeard J, Smith SR, Deighton M (2011) Microbial safety of air-dried and rewetted biosolids. J Water Health 9:403–414CrossRefGoogle Scholar
  81. 81.
    Schlatter D, Kinkel L, Thomashow L, Weller D, Paulitz T (2017) Disease suppressive soils: new insights from the soil microbiome. Phytopathology 107:1284–1297.  https://doi.org/10.1094/PHYTO-03-17-0111-RVW CrossRefGoogle Scholar
  82. 82.
    Hamdali H, Hafidi M, Virolle MJ, Ouhdouch Y (2008) Growth promotion and protection against damping-off of wheat by two rock phosphate solubilizing actinomycetes in a P-deficient soil under greenhouse conditions. Appl Soil Ecol 40:510–517.  https://doi.org/10.1016/j.apsoil.2008.08.001 CrossRefGoogle Scholar
  83. 83.
    Trivedi P, Sa T (2008) Pseudomonas corrugata (NRRL B-30409) mutants increased phosphate solubilization, organic acid production, and plant growth at lower temperatures. Curr Microbiol 56:140–144.  https://doi.org/10.1007/s00284-007-9058-8 CrossRefGoogle Scholar
  84. 84.
    Bakker PAHM, Pieterse CMJ, van Loon LC (2007) Induced systemic resistance by fluorescent Pseudomonas spp. Phytopathology 97:239–243.  https://doi.org/10.1094/PHYTO-97-2-0239 CrossRefGoogle Scholar
  85. 85.
    Viaene T, Langendries S, Beirinckx S et al (2016) Streptomyces as a plant’s best friend? FEMS Microbiol Ecol 92:fiw119.  https://doi.org/10.1093/femsec/fiw119 CrossRefGoogle Scholar
  86. 86.
    Chen M-H, Jack ALH, McGuire IC, Nelson EB (2012) Seed-colonizing bacterial communities associated with the suppression of Pythium seedling disease in a municipal biosolids compost. Phytopathology 102:478–489.  https://doi.org/10.1094/PHYTO-08-11-0240-R CrossRefGoogle Scholar
  87. 87.
    Chen M-H, Nelson EB (2008) Seed-colonizing microbes from municipal biosolids compost suppress Pythium ultimum damping-off on different plant species. Phytopathology 98:1012–1018.  https://doi.org/10.1094/PHYTO-98-9-1012 CrossRefGoogle Scholar
  88. 88.
    Bruce JB, West SA, Griffin AS (2017) Bacteriocins and the assembly of natural Pseudomonas fluorescens populations. J Evol Biol 30:352–360.  https://doi.org/10.1111/jeb.13010 CrossRefGoogle Scholar
  89. 89.
    Watve MG, Tickoo R, Jog MM, Bhole BD (2001) How many antibiotics are produced by the genus Streptomyces? Arch Microbiol 176:386–390.  https://doi.org/10.1007/s002030100345 CrossRefGoogle Scholar
  90. 90.
    Essarioui A, LeBlanc N, Kistler HC, Kinkel LL (2017) Plant community richness mediates inhibitory interactions and resource competition between Streptomyces and Fusarium populations in the rhizosphere. Microb Ecol 74:157–167.  https://doi.org/10.1007/s00248-016-0907-5 CrossRefGoogle Scholar
  91. 91.
    Cytryn E, Kautsky L, Ofek M, Mandelbaum RT, Minz D (2011) Short-term structure and functional changes in bacterial community composition following amendment with biosolids compost. Appl Soil Ecol 48:160–167.  https://doi.org/10.1016/j.apsoil.2011.03.010 CrossRefGoogle Scholar
  92. 92.
    Reardon CL, Wuest SB (2016) Soil amendments yield persisting effects on the microbial communities—a 7-year study. Appl Soil Ecol 101:107–116.  https://doi.org/10.1016/j.apsoil.2015.12.013 CrossRefGoogle Scholar
  93. 93.
    Sullivan TS, Stromberger ME, Paschke MW (2006) Parallel shifts in plant and soil microbial communities in response to biosolids in a semi-arid grassland. Soil Biol Biochem 38:449–459.  https://doi.org/10.1016/j.soilbio.2005.05.018 CrossRefGoogle Scholar
  94. 94.
    Gessler F, Böhnel H (2006) Persistence and mobility of a Clostridium botulinum spore population introduced to soil with spiked compost: persistence and mobility of Clostridium botulinum. FEMS Microbiol Ecol 58:384–393.  https://doi.org/10.1111/j.1574-6941.2006.00183.x CrossRefGoogle Scholar
  95. 95.
    Hopwood DA (2007) Streptomyces in nature and medicine: the antibiotic makers. Oxford University Press, Oxford, New YorkGoogle Scholar
  96. 96.
    Sharma-Poudyal D, Schlatter D, Yin C, Hulbert S, Paulitz T (2017) Long-term no-till: a major driver of fungal communities in dryland wheat cropping systems. PLoS One 12:e0184611.  https://doi.org/10.1371/journal.pone.0184611 CrossRefGoogle Scholar
  97. 97.
    Smith CR, Blair PL, Boyd C, Cody B, Hazel A, Hedrick A, Kathuria H, Khurana P, Kramer B, Muterspaw K, Peck C, Sells E, Skinner J, Tegeler C, Wolfe Z (2016) Microbial community responses to soil tillage and crop rotation in a corn/soybean agroecosystem. Ecol Evol 6:8075–8084.  https://doi.org/10.1002/ece3.2553 CrossRefGoogle Scholar

Copyright information

© This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply 2019

Authors and Affiliations

  • Daniel C. Schlatter
    • 1
  • Narayan C. Paul
    • 2
  • Devendra H. Shah
    • 2
  • William F. Schillinger
    • 3
  • Andy I. Bary
    • 4
  • Brenton Sharratt
    • 5
  • Timothy C. Paulitz
    • 1
    Email author
  1. 1.Wheat Health, Genetics and Quality Research UnitUSDA-ARSPullmanUSA
  2. 2.Department of Veterinary Microbiology and Pathology, College of Veterinary MedicineWashington State UniversityPullmanUSA
  3. 3.Department of Crop and Soil SciencesWashington State UniversityPullmanUSA
  4. 4.Puyallup Research and Extension CenterWashington State UniversityPuyallupUSA
  5. 5.Northwest Sustainable Agroecosystems Research UnitUSDA-ARSPullmanUSA

Personalised recommendations