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Soil microbiomes and one health

Abstract

The concept of one health highlights that human health is not isolated but connected to the health of animals, plants and environments. In this Review, we demonstrate that soils are a cornerstone of one health and serve as a source and reservoir of pathogens, beneficial microorganisms and the overall microbial diversity in a wide range of organisms and ecosystems. We list more than 40 soil microbiome functions that either directly or indirectly contribute to soil, plant, animal and human health. We identify microorganisms that are shared between different one health compartments and show that soil, plant and human microbiomes are perhaps more interconnected than previously thought. Our Review further evaluates soil microbial contributions to one health in the light of dysbiosis and global change and demonstrates that microbial diversity is generally positively associated with one health. Finally, we present future challenges in one health research and formulate recommendations for practice and evaluation.

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Fig. 1: The link between soil, plant, animal and human microbiomes.
Fig. 2: How the soil microbiome influences one health.
Fig. 3: Factors governing the soil microbial contributions to one health.

Data availability

The data for microbiome composition in Fig. 1 are available in Dryad: https://datadryad.org/stash/share/CPLkD5krQ1-MgaaiI3T0eIyGCTolnsN6tgK0sJ5GlQg.

References

  1. Berg, G. et al. Microbiome definition re-visited: old concepts and new challenges. Microbiome 8, 1–22 (2020). This article proposes a definition of the microbiome by distinguishing the terms microbiome and microbiota, and provides a discussion on the heterogeneity and dynamics of microbiomes in time and space.

    Article  Google Scholar 

  2. Berendsen, R. L., Pieterse, C. M. J. & Bakker, P. A. H. M. The rhizosphere microbiome and plant health. Trends Plant. Sci. 17, 478–486 (2012).

    CAS  PubMed  Article  Google Scholar 

  3. Carthey, A. J. R., Gillings, M. R. & Blumstein, D. T. The extended genotype: microbially mediated olfactory communication. Trends Ecol. Evol. 33, 885–894 (2018).

    PubMed  Article  Google Scholar 

  4. Singh, B. K., Liu, H. & Trivedi, P. Eco-holobiont: a new concept to identify drivers of host-associated microorganisms. Environ. Microbiol. 22, 564–567 (2020).

    PubMed  Article  Google Scholar 

  5. Adair, K. L., Wilson, M., Bost, A. & Douglas, A. E. Microbial community assembly in wild populations of the fruit fly Drosophila melanogaster. ISME J. 12, 959–972 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  6. Trinh, P., Zaneveld, J. R., Safranek, S. & Rabinowitz, P. M. One health relationships between human, animal, and environmental microbiomes: a mini-review. Front. Public Health 6, 1–9 (2018).

    Article  Google Scholar 

  7. Mackenzie, J., McKinnon, M. & Jeggo, M. in Confronting Emerging Zoonoses: The One Health Paradigm (eds Yamada, A. et al.) 1–254 (2014).

  8. Destoumieux-Garzón, D. et al. The one health concept: 10 years old and a long road ahead. Front. Vet. Sci. 5, 1–13 (2018).

    Article  Google Scholar 

  9. Rüegg, S. R. et al. A systems approach to evaluate one health initiatives. Front. Vet. Sci. 5, 1–18 (2018).

    Article  Google Scholar 

  10. Bar-On, Y. M., Phillips, R. & Milo, R. The biomass distribution on Earth. Proc. Natl Acad. Sci. USA 115, 6506–6511 (2018). This article provides an assessment of the overall biomass composition of the biosphere and shows that terrestrial biomass is about two orders of magnitude higher than marine biomass.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  11. van der Heijden, M. G. A., Bardgett, R. D. & Van Straalen, N. M. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol. Lett. 11, 296–310 (2008). This article summarizes various roles of soil microorganisms in terrestrial ecosystems and highlights that soil microorganisms must be considered as important drivers of plant diversity and productivity.

    PubMed  Article  Google Scholar 

  12. Bardgett, R. D. & van der Putten, W. H. Belowground biodiversity and ecosystem functioning. Nature 515, 505–511 (2014). This review emphasizes the diversity of microorganisms and animals that live in soils and how microorganisms contribute to ecosystem functioning.

    CAS  PubMed  Article  Google Scholar 

  13. Fierer, N. Embracing the unknown: disentangling the complexities of the soil microbiome. Nat. Rev. Microbiol. 15, 579–590 (2017). This review highlights the complexity of soil microorganisms and the roles they play in various biogeochemical cycles.

    CAS  PubMed  Article  Google Scholar 

  14. Dias, P. C. Sources and sinks in population biology. Trends Ecol. Evol. 11, 326–330 (1996).

    CAS  PubMed  Article  Google Scholar 

  15. Edwards, J. et al. Structure, variation, and assembly of the root-associated microbiomes of rice. Proc. Natl Acad. Sci. USA 112, E911–E920 (2015). This article provides detailed evidence on the assembly and recruitment of the root-associated microbiomes.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  16. Walsh, C. M., Becker-Uncapher, I., Carlson, M. & Fierer, N. Variable influences of soil and seed-associated bacterial communities on the assembly of seedling microbiomes. ISME J. 15, 2748–2762 (2021).

    CAS  PubMed  Article  Google Scholar 

  17. Rochefort, A. et al. Transmission of seed and soil microbiota to seedling. mSystems 6, e0044621 (2021).

    PubMed  Article  Google Scholar 

  18. Bergna, A. et al. Tomato seeds preferably transmit plant beneficial endophytes. Phytobiomes J. 2, 183–193 (2018).

    Article  Google Scholar 

  19. Abdelfattah, A., Wisniewski, M., Schena, L. & Tack, A. J. M. Experimental evidence of microbial inheritance in plants and transmission routes from seed to phyllosphere and root. Environ. Microbiol. 23, 2199–2214 (2021).

    CAS  PubMed  Article  Google Scholar 

  20. Bulgarelli, D., Schlaeppi, K., Spaepen, S., van Themaat, E. V. L. & Schulze-Lefert, P. Structure and functions of the bacterial microbiota of plants. Annu. Rev. Plant Biol. 64, 807–838 (2013). This review highlights the composition of plant-associated microbiota and summarizes the factors that drive their structure and functions.

    CAS  PubMed  Article  Google Scholar 

  21. Fitzpatrick, C. R. et al. Assembly and ecological function of the root microbiome across angiosperm plant species. Proc. Natl Acad. Sci. USA https://doi.org/10.1073/pnas.1717617115 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  22. Arumugam, M. et al. Enterotypes of the human gut microbiome. Nature 473, 174–180 (2011). This article performs a metagenomic analysis of samples from four countries and reveals the factors that drive the enterotypes of the human gut microbiome.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  23. Amat, S., Holman, D. B., Timsit, E., Schwinghamer, T. & Alexander, T. W. Evaluation of the nasopharyngeal microbiota in beef cattle transported to a feedlot, with a focus on lactic acid-producing bacteria. Front. Microbiol. 10, 1988 (2019).

    PubMed  PubMed Central  Article  Google Scholar 

  24. Trivedi, P., Leach, J. E., Tringe, S. G., Sa, T. & Singh, B. K. Plant–microbiome interactions: from community assembly to plant health. Nat. Rev. Microbiol. 18, 607–621 (2020). This review summarizes the genetic, biochemical and metabolic interactions between the host plant and its associated microbiomes.

    CAS  PubMed  Article  Google Scholar 

  25. Mahaney, W. C. & Krishnamani, R. Understanding geophagy in animals: standard procedures for sampling soils. J. Chem. Ecol. 29, 1503–1523 (2003).

    CAS  PubMed  Article  Google Scholar 

  26. Liddicoat, C. et al. Naturally-diverse airborne environmental microbial exposures modulate the gut microbiome and may provide anxiolytic benefits in mice. Sci. Total Environ. 701, 134684 (2020).

    CAS  PubMed  Article  Google Scholar 

  27. Ottman, N. et al. Soil exposure modifies the gut microbiota and supports immune tolerance in a mouse model. J. Allergy Clin. Immunol. 143, 1198–1206.e12 (2019).

    CAS  PubMed  Article  Google Scholar 

  28. Attwood, G. T. et al. Applications of the soil, plant and rumen microbiomes in pastoral agriculture. Front. Nutr. 6, 1–17 (2019).

    Article  CAS  Google Scholar 

  29. Mcgrath, D., Poole, D. B. R., Fleming, G. A. & Sinnott, J. Soil ingestion by grazing sheep. Ir. J. Agric. Res. 21, 135–145 (1982).

    Google Scholar 

  30. Healy, W. B. Ingestion of soil by dairy cows. N. Z. J. Agric. Res. 11, 487–499 (2012).

    Article  Google Scholar 

  31. Ross, A. A., Müller, K. M., Weese, J. S. & Neufeld, J. D. Comprehensive skin microbiome analysis reveals the uniqueness of human skin and evidence for phylosymbiosis within the class Mammalia. Proc. Natl Acad. Sci. USA 115, E5786–E5795 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  32. Bindari, Y. R., Moore, R. J., Van, T. T. H., Brown, S. W. W. & Gerber, P. F. Microbial taxa in dust and excreta associated with the productive performance of commercial meat chicken flocks. Anim. Microbiome https://doi.org/10.1186/s42523-021-00127-y (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  33. Sun, H., Peng, K., Xue, M. & Liu, J. Metagenomics analysis revealed the distinctive ruminal microbiome and resistive profiles in dairy buffaloes. Anim. Microbiome 3, 1–13 (2021).

    Article  CAS  Google Scholar 

  34. Sing, D. & Sing, C. F. Impact of direct soil exposures from airborne dust and geophagy on human health. Int. J. Environ. Res. Public Health https://doi.org/10.3390/ijerph7031205 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  35. Nyanza, E. C., Joseph, M., Premji, S. S., Thomas, D. S. K. & Mannion, C. Geophagy practices and the content of chemical elements in the soil eaten by pregnant women in artisanal and small scale gold mining communities in Tanzania. BMC Pregnancy Childbirth 14, 1–10 (2014).

    Article  Google Scholar 

  36. Pearson, A. L. et al. Associations detected between measures of neighborhood environmental conditions and human microbiome diversity. Sci. Total Environ. 745, 141029 (2020).

    CAS  PubMed  Article  Google Scholar 

  37. Liddicoat, C. et al. Ambient soil cation exchange capacity inversely associates with infectious and parasitic disease risk in regional Australia. Sci. Total Environ. 626, 117–125 (2018).

    CAS  PubMed  Article  Google Scholar 

  38. Stanaway, I. B. et al. Human oral buccal microbiomes are associated with farmworker status and azinphos-methyl agricultural pesticide exposure. Appl. Environ. Microbiol. 83, e02149-16 (2017).

    PubMed  Article  Google Scholar 

  39. Shukla, S. K. et al. The nasal microbiota of dairy farmers is more complex than oral microbiota, reflects occupational exposure, and provides competition for staphylococci. PLoS ONE 12, 1–18 (2017).

    Google Scholar 

  40. Doran, J. W. & Zeiss, M. R. Soil health and sustainability: managing the biotic component of soil quality. Appl. Soil Ecol. 15, 3–11 (2000).

    Article  Google Scholar 

  41. McBratney, A. B., Field, D. J. & Koch, A. The dimensions of soil security. Geoderma 213, 203–213 (2014).

    Article  Google Scholar 

  42. Lehmann, J., Bossio, D. A., Kögel-Knabner, I. & Rillig, M. C. The concept and future prospects of soil health. Nat. Rev. Earth Environ. 1, 544–553 (2020).

    PubMed  PubMed Central  Article  Google Scholar 

  43. Bünemann, E. K. et al. Soil quality — a critical review. Soil Biol. Biochem. 120, 105–125 (2018). This review provides a critical appraisal of soil quality and summarizes a wide variety of indicators.

    Article  CAS  Google Scholar 

  44. Fierer, N., Wood, S. A. & Bueno de Mesquita, C. P. How microbes can, and cannot, be used to assess soil health. Soil Biol. Biochem. 153, 108111 (2021).

    CAS  Article  Google Scholar 

  45. Garland, G. et al. Crop cover is more important than rotational diversity for soil multifunctionality and cereal yields in European cropping systems. Nat. Food 2, 28–37 (2021).

    Article  Google Scholar 

  46. Tamburini, G. et al. Agricultural diversification promotes multiple ecosystem services without compromising yield. Sci. Adv. 6, eaba1715 (2020).

    PubMed  PubMed Central  Article  Google Scholar 

  47. Edlinger, A., Garland, G. & Banerjee, S. Agricultural management and pesticide use reduce the functioning of benecial plant symbionts. Nat. Ecol. Evol. https://doi.org/10.1038/s41559-022-01799-8 (2022). This study demonstrates that pesticides reduce the natural nutrient uptake capacity of one of the oldest and most widespread symbionts of plants.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Sallach, J. B., Thirkell, T. J., Field, K. J. & Carter, L. J. The emerging threat of human-use antifungals in sustainable and circular agriculture schemes. Plants People Planet 3, 685–693 (2021).

    Article  Google Scholar 

  49. Banerjee, S. et al. Agricultural intensification reduces microbial network complexity and the abundance of keystone taxa in roots. ISME J. 13, 1722–1736 (2019).

    PubMed  PubMed Central  Article  Google Scholar 

  50. Schmidt, M. W. I. et al. Persistence of soil organic matter as an ecosystem property. Nature 478, 49–56 (2011). This review highlights that the stability of SOM is determined by microhabitat properties.

    CAS  PubMed  Article  Google Scholar 

  51. Liang, C. & Balser, T. C. Microbial production of recalcitrant organic matter in global soils: implications for productivity and climate policy. Nat. Rev. Microbiol. 9, 75 (2011).

    CAS  PubMed  Article  Google Scholar 

  52. Schimel, J. P. & Schaeffer, S. M. Microbial control over carbon cycling in soil. Front. Microbiol. 3, 1–11 (2012). This review discusses the role of microorganisms in soil carbon cycling and highlights the ecology of microorganisms in terms of broad and narrow processes in soil.

    Article  CAS  Google Scholar 

  53. Kallenbach, C. M., Frey, S. D. & Grandy, A. S. Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls. Nat. Commun. 7, 1–10 (2016). This study provides evidence that soil microbial biomass can be a chemically diverse yet stable pool of soil carbon.

    Article  CAS  Google Scholar 

  54. Banerjee, S. et al. Microbial interkingdom associations across soil depths reveal network connectivity and keystone taxa linked to soil fine-fraction carbon content. Agric. Ecosyst. Environ. 320, 107559 (2021).

    CAS  Article  Google Scholar 

  55. Bender, S. F., Wagg, C. & van der Heijden, M. G. A. An underground revolution: biodiversity and soil ecological engineering for agricultural sustainability. Trends Ecol. Evol. 31, 440–452 (2016).

    PubMed  Article  Google Scholar 

  56. Alori, E. T., Glick, B. R. & Babalola, O. O. Microbial phosphorus solubilization and its potential for use in sustainable agriculture. Front. Microbiol. 8, 1–8 (2017).

    Article  Google Scholar 

  57. Saha, M. et al. Microbial siderophores and their potential applications: a review. Environ. Sci. Pollut. Res. 23, 3984–3999 (2015).

    Article  CAS  Google Scholar 

  58. Brevik, E. et al. Soil and human health: current status and future needs. Air Soil Water Res. 13, 1–23 (2020).

    Article  Google Scholar 

  59. Lugtenberg, B. & Kamilova, F. Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol. 63, 541–556 (2009). This review discusses the rhizosphere as a habitat and summarizes various beneficial roles of the rhizosphere microbiota.

    CAS  PubMed  Article  Google Scholar 

  60. van der Heijden, M. G. A., Martin, F. M., Selosse, M. A. & Sanders, I. R. Mycorrhizal ecology and evolution: the past, the present, and the future. N. Phytol. 205, 1406–1423 (2015).

    Article  CAS  Google Scholar 

  61. Richardson, A. E., Barea, J. M., McNeill, A. M. & Prigent-Combaret, C. Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321, 305–339 (2009).

    CAS  Article  Google Scholar 

  62. Berg, G., Grube, M., Schloter, M. & Smalla, K. The plant microbiome and its importance for plant and human health. Front. Microbiol. 5, 1–2 (2014).

    Google Scholar 

  63. Parniske, M. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat. Rev. Microbiol. 6, 763–75 (2008).

    CAS  PubMed  Article  Google Scholar 

  64. Smith, S. & Read, D. Mycorrhizal Symbiosis (Elsevier, 2008).

  65. Hoeksema, J. D. et al. A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol. Lett. 13, 394–407 (2010).

    PubMed  Article  Google Scholar 

  66. Lekberg, Y. & Koide, R. T. Is plant performance limited by abundance of arbuscular mycorrhizal fungi? A meta-analysis of studies published between 1988 and 2003. N. Phytol. 168, 189–204 (2005).

    CAS  Article  Google Scholar 

  67. Salomon, M. J. et al. Global evaluation of commercial arbuscular mycorrhizal inoculants under greenhouse and field conditions. Appl. Soil Ecol. 169, 104225 (2022).

    Article  Google Scholar 

  68. Gill, S. S. et al. Piriformospora indica: potential and significance in plant stress tolerance. Front. Microbiol. 7, 332 (2016).

    PubMed  PubMed Central  Article  Google Scholar 

  69. Geisen, S. et al. Soil protists: a fertile frontier in soil biology research. FEMS Microbiol. Rev. 42, 293–323 (2018).

    CAS  PubMed  Article  Google Scholar 

  70. Wall, D. H., Nielsen, U. N. & Six, J. Soil biodiversity and human health. Nature 528, 69–76 (2015).

    CAS  PubMed  Article  Google Scholar 

  71. Backer, R. et al. Plant growth-promoting rhizobacteria: context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture. Front. Plant Sci. 871, 1–17 (2018).

    Google Scholar 

  72. Philippot, L., Raaijmakers, J. M., Lemanceau, P. & Van Der Putten, W. H. Going back to the roots: the microbial ecology of the rhizosphere. Nat. Rev. Microbiol. 11, 789–799 (2013). This review highlights the importance of understanding the rhizosphere and its microbiota for sustainable agriculture and climate change mitigation.

    CAS  PubMed  Article  Google Scholar 

  73. Schlaeppi, K. & Bulgarelli, D. The plant microbiome at work. Mol. Plant Microbe Interact. 28, 212–217 (2015).

    CAS  PubMed  Article  Google Scholar 

  74. Compant, S., Samad, A., Faist, H. & Sessitsch, A. A review on the plant microbiome: ecology, functions, and emerging trends in microbial application. J. Adv. Res. 19, 29–37 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  75. Fitzpatrick, C. R. et al. The plant microbiome: from ecology to reductionism and beyond. Annu. Rev. Microbiol. 74, 81–100 (2020).

    CAS  PubMed  Article  Google Scholar 

  76. Deshani Igalavithana, A. et al. Assessment of soil health in urban agriculture: soil enzymes and microbial properties. Sustainability 9, 310 (2017).

    Article  CAS  Google Scholar 

  77. van der Heijden, M. G. A., Bruin, S., De, Luckerhoff, L., van Logtestijn, R. S. & Schlaeppi, K. A widespread plant–fungal–bacterial symbiosis promotes plant biodiversity, plant nutrition and seedling recruitment. ISME J. 10, 1–11 (2016).

    Article  CAS  Google Scholar 

  78. Zhang, J. et al. NRT1.1B is associated with root microbiota composition and nitrogen use in field-grown rice. Nat. Biotechnol. 37, 676–684 (2019).

    CAS  PubMed  Article  Google Scholar 

  79. Van Elsas, J. D. et al. Microbial diversity determines the invasion of soil by a bacterial pathogen. Proc. Natl Acad. Sci. USA 109, 1159–1164 (2012). This study shows an inverse relationship between soil microbial diversity and survival of the invading species E. coli O157:H7. The study reveals a lack of competitive ability of invading pathogen in species-rich environments.

    PubMed  PubMed Central  Article  Google Scholar 

  80. Wagg, C., Schlaeppi, K., Banerjee, S., Kuramae, E. E. & van der Heijden, M. G. A. Fungal–bacterial diversity and microbiome complexity predict ecosystem functioning. Nat. Commun. 10, 1–10 (2019).

    CAS  Article  Google Scholar 

  81. Fitzpatrick, C. R., Mustafa, Z. & Viliunas, J. Soil microbes alter plant fitness under competition and drought. J. Evol. Biol. 32, 438–450 (2019).

    PubMed  Article  Google Scholar 

  82. Expósito, R. G., de Bruijn, I., Postma, J. & Raaijmakers, J. M. Current insights into the role of rhizosphere bacteria in disease suppressive soils. Front. Microbiol. 8, 1–12 (2017).

    Google Scholar 

  83. Schlatter, D., Kinkel, L., Thomashow, L., Weller, D. & Paulitz, T. Disease suppressive soils: new insights from the soil microbiome. Phytopathology 107, 1284–1297 (2017).

    PubMed  Article  Google Scholar 

  84. McSpadden Gardener, B. B. & Weller, D. M. Changes in populations of rhizosphere bacteria associated with take-all disease of wheat. Appl. Environ. Microbiol. 67, 4414–4425 (2001).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  85. Mendes, R. et al. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332, 1097–1100 (2011).

    CAS  PubMed  Article  Google Scholar 

  86. Kikuchi, Y., Hosokawa, T. & Fukatsu, T. An ancient but promiscuous host–symbiont association between Burkholderia gut symbionts and their heteropteran hosts. ISME J. 5, 446–460 (2010).

    PubMed  PubMed Central  Article  Google Scholar 

  87. Hannula, S. E., Zhu, F., Heinen, R. & Bezemer, T. M. Foliar-feeding insects acquire microbiomes from the soil rather than the host plant. Nat. Commun. 10, 1–9 (2019). This study shows soil as the reservoir of microorganisms for leaf-feeding caterpillars and reveals the connection between the soil and insect microbiomes.

    CAS  Article  Google Scholar 

  88. Kikuchi, Y. et al. Symbiont-mediated insecticide resistance. Proc. Natl Acad. Sci. USA 109, 8618–8622 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  89. Bruijning, M., Henry, L. P., Forsberg, S. K. G., Metcalf, C. J. E. & Ayroles, J. F. Natural selection for imprecise vertical transmission in host–microbiota systems. Nat. Ecol. Evol. 6, 77–87 (2021).

    PubMed  Article  Google Scholar 

  90. Wilschut, R. A. & Geisen, S. Nematodes as drivers of plant performance in natural systems. Trends Plant Sci. 26, 237–247 (2021).

    CAS  PubMed  Article  Google Scholar 

  91. Reese, A. T. & Dunn, R. R. Drivers of microbiome biodiversity: a review of general rules, feces, and ignorance. mBio 9, e01294-18 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  92. Peixoto, R. S., Harkins, D. M. & Nelson, K. E. Advances in microbiome research for animal health. Annu. Rev. Anim. Biosci. 9, 289–311 (2021).

    CAS  PubMed  Article  Google Scholar 

  93. UIA. Soil-borne diseases in animals. The Encyclopedia of World Problems http://encyclopedia.uia.org/en/problem/141320 (2021).

  94. Lerner, P. Nocardiosis. Clin. Infect. Dis. 22, 891–905 (1996).

    CAS  PubMed  Article  Google Scholar 

  95. Costa, J. L. N. et al. Outbreak of malignant oedema in sheep caused by Clostridium sordellii, predisposed by routine vaccination. Vet. Rec. 160, 594–595 (2007).

    CAS  PubMed  Article  Google Scholar 

  96. Young, S. L., Sherman, P. W., Lucks, J. B. & Pelto, G. H. Why on earth?: evaluating hypotheses about the physiological functions of human geophagy. Q. Rev. Biol. 86, 97–120 (2011).

    PubMed  Article  Google Scholar 

  97. Blum, W. E. H., Zechmeister-Boltenstern, S. & Keiblinger, K. M. Does soil contribute to the human gut microbiome? Microorganisms 7, 287 (2019).

    PubMed Central  Article  Google Scholar 

  98. Hanski, I. et al. Environmental biodiversity, human microbiota, and allergy are interrelated. Proc. Natl Acad. Sci. USA 109, 8334–8339 (2012). This study reveals the connection between allergy in humans and microbial diversity in environments.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  99. Wills-Karp, M., Santeliz, J. & Karp, C. L. The germless theory of allergic disease: revisiting the hygiene hypothesis. Nat. Rev. Immunol. 1, 69–75 (2001).

    CAS  PubMed  Article  Google Scholar 

  100. Yazdanbakhsh, M., Kremsner, P. G. & Van Ree, R. Parasites and the hygiene hypothesis. Sci 296, 490–494 (2002).

    CAS  Article  Google Scholar 

  101. Hopping, K. A., Chignell, S. M. & Lambin, E. F. The demise of caterpillar fungus in the Himalayan region due to climate change and overharvesting. Proc. Natl Acad. Sci. USA 115, 11489–11494 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  102. Hirt, H. Healthy soils for healthy plants for healthy humans. EMBO Rep. 21, 1–5 (2020).

    Article  CAS  Google Scholar 

  103. Brevik, E. C. & Burgess, L. C. The 2012 fungal meningitis outbreak in the United States: connections between soils and human health. Soil Horiz. 54, 1–4 (2013).

    Google Scholar 

  104. Steffan, J. J., Brevik, E. C., Burgess, L. C. & Cerdà, A. The effect of soil on human health: an overview. Eur. J. Soil Sci. 69, 159–171 (2018).

    CAS  PubMed  Article  Google Scholar 

  105. Loukas, A. et al. Hookworm infection. Nat. Rev. Dis. Primers 2, 1–18 (2016).

    Article  Google Scholar 

  106. Rangel, J. M., Sparling, P. H., Crowe, C., Griffin, P. M. & Swerdlow, D. L. Epidemiology of O157:H7 outbreaks, United States, 1982–2002. Emerg. Infect. Dis. 11, 603–609 (2005).

    PubMed  PubMed Central  Article  Google Scholar 

  107. Franz, E. et al. Manure-amended soil characteristics affecting the survival of E. coli O157:H7 in 36 Dutch soils. Environ. Microbiol. 10, 313–327 (2008).

    CAS  PubMed  Article  Google Scholar 

  108. Berg, G., Eberl, L. & Hartmann, A. The rhizosphere as a reservoir for opportunistic human pathogenic bacteria. Environ. Microbiol. 7, 1673–1685 (2005).

    CAS  PubMed  Article  Google Scholar 

  109. Guzman-Otazo, J. I. et al. Diarrheal bacterial pathogens and multi-resistant enterobacteria in the Choqueyapu River in La Paz, Bolivia. PLoS ONE https://doi.org/10.1371/journal.pone.0210735 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  110. Barnes, G., Saunders, D. G. O. & Williamson, T. Banishing barberry: the history of Berberis vulgaris prevalence and wheat stem rust incidence across Britain. Plant Pathol. 69, 1193–1202 (2020).

    Article  Google Scholar 

  111. 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. 75, 5111–5120 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  112. Chu, H. et al. Soil bacterial diversity in the Arctic is not fundamentally different from that found in other biomes. Environ. Microbiol. 12, 2998–3006 (2010).

    CAS  PubMed  Article  Google Scholar 

  113. Wei, Y. et al. Does pH matter for ecosystem multifunctionality? An empirical test in a semi-arid grassland on the Loess Plateau. Funct. Ecol. https://doi.org/10.1111/1365-2435.14057 (2022).

    Article  Google Scholar 

  114. Svenningsen, N. B. et al. Suppression of the activity of arbuscular mycorrhizal fungi by the soil microbiota. ISME J. 12, 1296–1307 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  115. Sul, W. J. et al. Tropical agricultural land management influences on soil microbial communities through its effect on soil organic carbon. Soil Biol. Biochem. 65, 33–38 (2013).

    CAS  Article  Google Scholar 

  116. Geyer, K. M., Kyker-Snowman, E., Grandy, A. S. & Frey, S. D. Microbial carbon use efficiency: accounting for population, community, and ecosystem-scale controls over the fate of metabolized organic matter. Biogeochemistry 127, 173–188 (2016).

    CAS  Article  Google Scholar 

  117. Rillig, M. C. et al. The role of multiple global change factors in driving soil functions and microbial biodiversity. Science 366, 886–890 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  118. Cavicchioli, R. et al. Scientists’ warning to humanity: microorganisms and climate change. Nat. Rev. Microbiol. 17, 569–586 (2019). This article is a consensus statement of scientists across the world and highlights how microorganisms affect climate change but are also affected by anthropogenic activities.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  119. Querejeta, J. I. et al. Lower relative abundance of ectomycorrhizal fungi under a warmer and drier climate is linked to enhanced soil organic matter decomposition. N. Phytol. 232, 1399–1413 (2021).

    CAS  Article  Google Scholar 

  120. Singh, B. K., Bardgett, R. D., Smith, P. & Reay, D. S. Microorganisms and climate change: terrestrial feedbacks and mitigation options. Nat. Rev. Microbiol. 8, 779–790 (2010). This review discusses microbial controls of terretrial greenhouse gas emissions and highlights the importance of soil microorganisms for climate change mitigation.

    CAS  PubMed  Article  Google Scholar 

  121. Delgado-Baquerizo, M. et al. The proportion of soil-borne pathogens increases with warming at the global scale. Nat. Clim. Chang. 10, 550–554 (2020). This study shows how elevated temperatures can increase the abundance of soil-borne plant pathogens, highlighting that climate change can lead to further prevalence of plant diseases.

    Article  Google Scholar 

  122. Romero, F. et al. Humidity and high temperature are important for predicting fungal disease outbreaks worldwide. N. Phytol. https://doi.org/10.1111/NPH.17340 (2021).

    Article  Google Scholar 

  123. Trivedi, P., Mattupalli, C., Eversole, K. & Leach, J. E. Enabling sustainable agriculture through understanding and enhancement of microbiomes. N. Phytol. 230, 2129–2147 (2021).

    Article  Google Scholar 

  124. Zhou, Z., Wang, C. & Luo, Y. Meta-analysis of the impacts of global change factors on soil microbial diversity and functionality. Nat. Commun. 11, 1–10 (2020).

    CAS  Article  Google Scholar 

  125. Jousset, A. et al. Where less may be more: how the rare biosphere pulls ecosystems strings. ISME J. 11, 853–862 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  126. Chen, Q. L. et al. Rare microbial taxa as the major drivers of ecosystem multifunctionality in long-term fertilized soils. Soil Biol. Biochem. 141, 107686 (2020).

    CAS  Article  Google Scholar 

  127. Persson, L. et al. Outside the safe operating space of the planetary boundary for novel entities. Environ. Sci. Technol. 56, 1510–1521 (2022).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  128. Larsson, D. G. J. & Flach, C. F. Antibiotic resistance in the environment. Nat. Rev. Microbiol. 20, 257–269 (2021).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  129. Kahn, L. H. Antimicrobial resistance: a one health perspective. Trans. R. Soc. Trop. Med. Hyg. 111, 255–260 (2017).

    PubMed  Article  Google Scholar 

  130. Hofer, U. The cost of antimicrobial resistance. Nat. Rev. Microbiol. 17, 3 (2018).

    Article  CAS  Google Scholar 

  131. McEwen, S. & Collignon, P. Antimicrobial resistance: a one health perspective. Microbiol. Spectr. 6, 1–26 (2018).

    Article  Google Scholar 

  132. Zhang, Y. J. et al. Transfer of antibiotic resistance from manure-amended soils to vegetable microbiomes. Environ. Int. 130, 104912 (2019).

    CAS  PubMed  Article  Google Scholar 

  133. Bahram, M. et al. Structure and function of the global topsoil microbiome. Nature https://doi.org/10.1038/s41586-018-0386-6 (2018). This study provides a global estimate of the structure and function of soil bacteria and fungi.

    Article  PubMed  Google Scholar 

  134. Matson, P. A. A., Parton, W. J. J., Power, A. G. G. & Swift, M. J. J. Agricultural intensification and ecosystem properties. Science 277, 504–509 (1997).

    CAS  PubMed  Article  Google Scholar 

  135. Babin, D., Leoni, C., Neal, A. L., Sessitsch, A. & Smalla, K. Editorial to the thematic topic “towards a more sustainable agriculture through managing soil microbiomes”. FEMS Microbiol. Ecol. 97, fiab094 (2021).

    CAS  PubMed  Article  Google Scholar 

  136. Tilman, D., Cassman, K. G., Matson, P. A., Naylor, R. & Polasky, S. Agricultural sustainability and intensive production practices. Nature 418, 671–677 (2002). This excellent review shows how the use of chemical fertilizers and pesticides increased with agricultural production over seven decades.

    CAS  PubMed  Article  Google Scholar 

  137. Oehl, F. et al. Impact of land use intensity on the species diversity of arbuscular mycorrhizal fungi in agroecosystems of Central Europe. Appl. Environ. Microbiol. 69, 2816–2824 (2003).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  138. Tsiafouli, M. A. et al. Intensive agriculture reduces soil biodiversity across Europe. Glob. Chang. Biol. 21, 973–985 (2015).

    PubMed  Article  Google Scholar 

  139. Verbruggen, E. et al. Positive effects of organic farming on below-ground mutualists: of mycorrhizal fungal comparison in agricultural communities soils. N. Phytol. 186, 968–979 (2010).

    CAS  Article  Google Scholar 

  140. Gossner, M. M. et al. Land-use intensification causes multitrophic homogenization of grassland communities. Nature 540, 266–269 (2016).

    CAS  PubMed  Article  Google Scholar 

  141. Gámez-Virués, S. et al. Landscape simplification filters species traits and drives biotic homogenization. Nat. Commun. 6, 1–8 (2015).

    Article  CAS  Google Scholar 

  142. Wittwer, R. A. et al. Organic and conservation agriculture promote ecosystem multifunctionality. Sci. Adv. 7, eabg6995 (2021).

    PubMed  PubMed Central  Article  Google Scholar 

  143. Fenner, K., Canonica, S., Wackett, L. P. & Elsner, M. Evaluating pesticide degradation in the environment: blind spots and emerging opportunities. Science 341, 752–758 (2013).

    CAS  PubMed  Article  Google Scholar 

  144. Silva, V. et al. Pesticide residues in European agricultural soils — a hidden reality unfolded. Sci. Total Environ. 653, 1532–1545 (2019).

    CAS  PubMed  Article  Google Scholar 

  145. Riedo, J. et al. Widespread occurrence of pesticides in organically managed agricultural soils — the ghost of a conventional agricultural past? Environ. Sci. Technol. 55, 2919–2928 (2021).

    CAS  PubMed  Article  Google Scholar 

  146. Delgado-Baquerizo, M. et al. Multiple elements of soil biodiversity drive ecosystem functions across biomes. Nat. Ecol. Evol. 4, 210–220 (2020).

    PubMed  Article  Google Scholar 

  147. Chen, T. et al. A plant genetic network for preventing dysbiosis in the phyllosphere. Nature 580, 653–657 (2020).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  148. Turnbaugh, P. J. et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444, 1027–1031 (2006). This article shows the link between gut microbiota and obesity in humans.

    PubMed  Article  Google Scholar 

  149. Breidenbach, A. et al. Microbial functional changes mark irreversible course of Tibetan grassland degradation. Nat. Commun. 13, 1–10 (2022).

    Article  CAS  Google Scholar 

  150. Hu, W. et al. Aridity-driven shift in biodiversity–soil multifunctionality relationships. Nat. Commun. 12, 1–15 (2021).

    Article  CAS  Google Scholar 

  151. Delgado-Baquerizo, M. et al. Global homogenization of the structure and function in the soil microbiome of urban greenspaces. Sci. Adv. 7, eabg5809 (2021).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  152. Van Boeckel, T. P. et al. Global trends in antimicrobial use in food animals. Proc. Natl Acad. Sci. USA 112, 5649–5654 (2015).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  153. Starr, E. P. et al. Stable-isotope-informed, genome-resolved metagenomics uncovers potential cross-kingdom interactions in rhizosphere soil. mSphere 6, e00085-21 (2021).

    PubMed Central  Article  Google Scholar 

  154. Trubl, G. et al. Soil viruses are underexplored players in ecosystem carbon processing. mSystems 3, e00076-18 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  155. Williamson, K. E., Fuhrmann, J. J., Wommack, K. E. & Radosevich, M. Viruses in soil ecosystems: an unknown quantity within an unexplored territory. Annu. Rev. Virol. 4, 201–219 (2017).

    CAS  PubMed  Article  Google Scholar 

  156. Flandroy, L. et al. The impact of human activities and lifestyles on the interlinked microbiota and health of humans and of ecosystems. Sci. Total Environ. 627, 1018–1038 (2018).

    CAS  PubMed  Article  Google Scholar 

  157. Tang, T. et al. Antibiotics increased host insecticide susceptibility via collapsed bacterial symbionts reducing detoxification metabolism in the brown planthopper, Nilaparvata lugens. J. Pest. Sci. 94, 757–767 (2021).

    CAS  Article  Google Scholar 

  158. Ryan, M. J. et al. Development of microbiome biobanks — challenges and opportunities. Trends Microbiol. 29, 89–92 (2021).

    CAS  PubMed  Article  Google Scholar 

  159. FAO, ITPS, GSBI, SCBD & EC. State of Knowledge of Soil Biodiversity - Status, challenges and potentialities (FAO, 2020).

  160. Jones, C. M. et al. Recently identified microbial guild mediates soil N2O sink capacity. Nat. Clim. Chang. 4, 801–805 (2014).

    CAS  Article  Google Scholar 

  161. Naylor, D. et al. Soil microbiomes under climate change and implications for carbon cycling. Annu. Rev. Environ. Resour. 45, 29–59 (2020).

    Article  Google Scholar 

  162. Banerjee, S. & Siciliano, S. D. Spatially tripartite interactions of denitrifiers in arctic ecosystems: activities, functional groups and soil resources. Environ. Microbiol. 14, 2601–2613 (2012).

    CAS  PubMed  Article  Google Scholar 

  163. Six, J., Elliott, E. T., Paustian, K. & Doran, J. W. Aggregation and soil organic matter accumulation in cultivated and native grassland soils. Soil Sci. Soc. Am. J. 62, 1367–1377 (1998).

    CAS  Article  Google Scholar 

  164. Anthony, M. A., Crowther, T. W., Maynard, D. S., van den Hoogen, J. & Averill, C. Distinct assembly processes and microbial communities constrain soil organic carbon formation. One Earth 2, 349–360 (2020).

    Article  Google Scholar 

  165. Wei, Z. et al. Trophic network architecture of root-associated bacterial communities determines pathogen invasion and plant health. Nat. Commun. 6, 1–9 (2015).

    Google Scholar 

  166. Harman, G. E., Howell, C. R., Viterbo, A., Chet, I. & Lorito, M. Trichoderma species — opportunistic, avirulent plant symbionts. Nat. Rev. Microbiol. 2, 43–56 (2004).

    CAS  PubMed  Article  Google Scholar 

  167. Saleem, M., Arshad, M., Hussain, S. & Bhatti, A. S. Perspective of plant growth promoting rhizobacteria (PGPR) containing ACC deaminase in stress agriculture. J. Ind. Microbiol. Biotechnol. 34, 635–648 (2007).

    CAS  PubMed  Article  Google Scholar 

  168. Morris, W. E., Uzal, F. A., Fattorini, F. R. & Terzolo, H. Malignant oedema associated with blood-sampling in sheep. Aust. Vet. J. 80, 280–281 (2002).

    CAS  PubMed  Article  Google Scholar 

  169. Zhu, T. et al. Bacterivore nematodes stimulate soil gross N transformation rates depending on their species. Biol. Fertil. Soils 54, 107–118 (2018).

    CAS  Article  Google Scholar 

  170. Edwards, A. A., Mathura, C. B. & Edwards, C. H. Effects of maternal geophagia on infant and juvenile rats. J. Natl Med. Assoc. 75, 895–902 (1983).

    CAS  PubMed  PubMed Central  Google Scholar 

  171. Gibbs, E. P. J. The evolution of One Health: a decade of progress and challenges for the future. Vet. Rec. 174, 85–91 (2014).

    PubMed  Article  Google Scholar 

  172. Dukes, T. W. That other branch of medicine: an historiography of veterinary medicine from a Canadian perspective. Can. Bull. Med. Hist. 17, 229–243 (2000).

    CAS  PubMed  Google Scholar 

  173. World Health Organization. Constitution. WHO https://www.who.int/about/governance/constitution (2021).

  174. Zegeye, E. K. et al. Selection, succession, and stabilization of soil microbial consortia. mSystems 4, e00055-19 (2019).

    PubMed  PubMed Central  Article  Google Scholar 

  175. Hooper, D. U. et al. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol. Monogr. 75, 3–35 (2005).

    Article  Google Scholar 

  176. Banerjee, S., Schlaeppi, K. & van der Heijden, M. G. A. Keystone taxa as drivers of microbiome structure and functioning. Nat. Rev. Microbiol. 16, 567–576 (2018). This commentary article highlights how keystone taxa can determine microbiome complexity and functioning. It also discusses the factors that determine their activities.

    CAS  PubMed  Article  Google Scholar 

  177. Nuñez, M. A., Horton, T. R. & Simberloff, D. Lack of belowground mutualisms hinders Pinaceae invasions. Ecology 90, 2352–2359 (2009).

    PubMed  Article  Google Scholar 

  178. Scheffer, M., Carpenter, S., Foley, J. A., Folke, C. & Walker, B. Catastrophic shifts in ecosystems. Nature 413, 591–596 (2001).

    CAS  PubMed  Article  Google Scholar 

  179. Clemmensen, K. E. et al. A tipping point in carbon storage when forest expands into tundra is related to mycorrhizal recycling of nitrogen. Ecol. Lett. 24, 1193–1204 (2021). This study shows that the role of mycorrhizal fungi in tundra soil carbon stocks is linked to a tipping point.

    PubMed  Article  Google Scholar 

  180. Gilbert, J. A. et al. Current understanding of the human microbiome. Nat. Med. 24, 392–400 (2018). This review provides an assessment of the human microbiome and challenges in our understanding.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

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Glossary

Microbiome

A characteristic microbial community occupying a reasonably well-defined habitat which has distinct physio-chemical properties. Thus, the microbiome is holistically defined as the microorganisms and their structural elements including nucleic acids, proteins, lipids, polysaccharides as well as various metabolites. Microbiomes also encompass microorganisms and their activities, including their spatiotemporal dynamics, which results in the formation of specific ecological niches.

Dysbiosis

An imbalance of microbiome structure and composition that is caused by host/environmental perturbations. It is usually associated with loss of taxonomic and/or functional diversity.

Microbial diversity

The number, relative abundance and composition of different microbial taxa present at a particular location. Thus, microbial diversity is a measure of microbial variation at the taxonomic, genetic, phylogenetic, functional and ecosystem levels. An optimal index should incorporate both richness and evenness.

Resistance

The ability of a microbiome to withstand a perturbation and remain unchanged in terms of community structure and composition.

Edaphic factors

Factors related to soil properties.

Global change factors

Natural or anthropogenic factors that are affecting environments globally.

Homogenization

A decline in the differences between ecosystems owing to external factors often resulting in reduced diversity and dominance of certain microbial groups.

Tipping points

Critical points that may occur owing to a single or a series of environmental perturbations and may either lead to dysbiosis or an alternative stable or healthy state.

Eubiosis

A healthy and stable state of microbiota with high diversity and abundance of commensals.

Redundancy

An important trait of microbiome stability whereby some taxa are functionally replaceable as other groups can continue their functions.

Resilience

The ability of a microbiome to endure a perturbation and return to a healthy state despite encountering initial changes in structure and composition.

Insurance

In this hypothesis, biodiversity insures ecosystems against perturbations and decline in functioning, as a diverse community guarantees that some groups will maintain functioning in the event that other groups fail.

Alternative stable state

A ‘healthy’ state that may occur owing to resilience in which the structure and composition of a microbiome are different from that of the original healthy state and yet the microbiome may continue to perform the same functions.

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Banerjee, S., van der Heijden, M.G.A. Soil microbiomes and one health. Nat Rev Microbiol (2022). https://doi.org/10.1038/s41579-022-00779-w

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