Transmission of microorganisms from soil to plant to gut

The composition of the human gut microbiome exhibits a discernible geographic pattern1. This phenomenon is largely influenced by diet and lifestyle, such as food fiber content, urban/rural environments, and exposure to farming2. The effects of these external factors on microbiome composition appear to be stronger than host traits such as relatedness and genetics2. Consequently, the microbiomes present in the soil and plant environment, in particular the edible plant parts, have recently been proposed as significant drivers of the taxonomic and functional diversity of the human gut microbiome3. Hence, the central aim of this perspective is to critically review if there is such a shared microbial reservoir across soil, plants, and the human gut.

The soil microbiome harbors at least 25% of the Earth’s total biodiversity4 and acts as a ‘microbial seed bank’ for the plant microbiome, in particular the roots (i.e., rhizosphere and endosphere)5 but also plant seeds and the phyllosphere, i.e., the aboveground plant parts including flowers and fruits6,7. Several examples have shown that fruit and vegetable-associated bacteria can enter the human gut and may contribute to gut microbial diversity8. In addition to direct transmission of microbes to the human gut via plant-based products, the metabolic content of edible plant products can also indirectly regulate the composition of the human gut microbiome9. Moreover, incidental or deliberate soil consumption (geophagy) has been proposed to provide health benefits, such as enhanced immunological resilience, through the modulation of the human gut microbiome10. Hence, the soil microbiome is regarded as a reservoir or ‘seed bank’ of microorganisms that can enter the human gut directly or indirectly via the plant5. But which microorganisms have been reported to transmit from soil to plant to gut? In turn, which members of the human gut microbiome are introduced back into the soil environment and on/in plant tissues through feces and food/water waste11. To gain a deeper understanding of this putative feedback loop, we will also review current knowledge of the reciprocal selection mechanisms and dynamics of the soil-plant-gut microbiome axis.

Mapping the distribution of microbiota across the soil-plant-human gut axis

To determine if there is a microbial reservoir along the soil-plant-human gut axis (Fig. 1), we first classified the microbes in these habitats as either specialists or generalists. Specialists are defined here as microbes confined to specific habitats, while generalists are those found across all habitats12. Being classified as habitat specialists does not preclude their existence in other habitats; rather, they are typically found in much lower abundance outside their primary habitat12. Among the generalist microbes, we define potential cross-kingdom microbiota as those with a high abundance across all three habitats13.

Fig. 1: Proposed distribution of microbes along the soil-plant-human gut microbiome axis.
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Soil, plants, and the human gut are each considered distinct habitats. Within each habitat, specific microbial communities known as habitat specialists are identified. Microbes that are distributed across all habitats are termed here as generalists. Based on their abundance and functions, a group of cross-kingdom microbiota is proposed among the generalist microbes. Created in BioRender. Ma, H. (2025) https://BioRender.com/b51e6if.

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Habitat specialists

Most soil microbes interact with plants, yet certain taxa involved in biogeochemical cycling prefer the soil habitat and typically do not rely on nutrient exchange with hosts as seen in human gut commensals or plant symbionts14 (Table 1). Therefore, soil habitat specialists are unlikely to traverse along the soil-plant-human gut microbiome axis. For instance, methanotrophs are soil bacteria that utilize methane as their sole source of carbon and energy15. They are most prevalent in submerged or water-saturated environments, such as wetlands16, but can also be found in termite guts when inhabiting methane-rich environments17. Similarly, Geobacter plays vital roles in soil elemental cycling and can be found in paddy farmland18, soils, and marine sediments, where they engage in syntrophic growth with methanogens19,20. Nitrosomonas, another example of a soil habitat specialist, is a bacterial genus that contributes to ammonia oxidation in aerated soils20. However, not all microbial genera involved in soil elemental cycling are absent in the human gut. For example, sulfate-reducing Desulfovibrio is typically found in soil but also frequently reported in the human gut21 and has been associated with gut microbiome dysbiosis22 and colonic diseases23.

Table 1 Examples of putative habitat specialists and generalists along the soil-plant-gut axis
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Plant microbiomes typically are formed by recruitment of a subset of the soil microbiome via the spatiotemporal release of exudates from plant seeds, roots, and leaves. Among these are microbial taxa that exhibit an intimate association with plants, here defined as plant habitat specialists. For instance, arbuscular mycorrhizal fungi (AMF) are obligate biotrophs reliant on plants for carbon supply to complete their life cycle24. This symbiotic relationship enhances plant nutrient acquisition (e.g., phosphate and nitrates) from the soil and can also boost disease resistance in plant hosts25. Similarly, N2-fixing rhizobia manifest their symbiosis through the formation of nodules, serving as miniature factories for nitrogen supply to the host plants, predominantly legumes26,27. Similarly, Epichloë, a genus of filamentous fungal endophytes, has co-evolved with cool-season grasses, forming long-term symbiotic associations28. Soil-borne plant pathogens can also be regarded as plant habitat specialists, proliferating upon encountering suitable hosts and entering back into dormancy in soil in the absence of their hosts29. Establishment of these associations involves intricate chemical communication between the plant and the soil microbiome via specific constituents in plant exudates. For example, phenolic acids such as salicylic acid, vanillic acid, can attract saprotrophic fungi like Fusarium species30, while strigolactones play a crucial role in the establishment of symbiotic relationships between plants and AMF31.

The composition of the human gut microbiome is continuously influenced by microbes entering via plant-based food and the environment. Unlike soil and plants, microbes considered as human gut habitat specialists typically possess anaerobic metabolism and adaptability to varying pH levels. The duodenum has a more acidic environment compared to the jejunum and ileum, while the large intestine maintains a relatively neutral pH32. Additionally, human gut habitat specialists should have the ability to utilize mucin, as the gut mucosa forms a protective barrier for epithelial cells and serves as an ecological niche for specific non-harmful members of the gut microbiome2,33. For example, Akkermansia muciniphila is well known for its mucin-degrading capabilities, which not only enable it to thrive in the gut environment but also to contribute to its role in maintaining gut barrier integrity and metabolic health33. A. muciniphila is highly abundant in the human gut34,35, and has been shown to diminish obesity, type 2 and type 1 diabetes mellitus, hepatic steatosis, intestinal inflammation, and various cancers in mice36. Furthermore, bile salts can be abundant in the small intestine, significantly influencing microbial colonization of the human gut37. For instance, the enzymatic preferences of bile salt hydrolases significantly affect the fitness of Lactobacillus and their colonization in humans38. Fermentation by gut microbes is crucial for converting luminal compounds into secondary metabolites and is considered an indicator of a healthy gut microbiome39,40. For example, Faecalibacterium prausnitzii, a major butyrate producer, contributes to gut health by fermenting fibers and producing short-chain fatty acids that have anti-inflammatory effects, which help suppress conditions like irritable bowel syndrome, obesity, and celia disease41. In this context, F. prausnitzii has been proposed as a biomarker for a healthy gut34,35,42. Other beneficial gut habitat specialists include Christensenella minuta, Anaerobutyricum soehngenii, and Oxalobacter formigenes36.

Habitat generalists

Habitat generalists should preferably possess specific features such as metabolic flexibility, stress tolerance, and genome plasticity, allowing them to adapt to the different environments43,44. For instance, Clostridium spp. encompasses many habitat generalists such as C. cadaveris and C. senegalense, characterized by its metabolic flexibility, can thrive in diverse environments (Table 1)45. In soil and plants, Clostridium species can exhibit beneficial functions such as biological nitrogen fixation and phosphate solubilization46. In the human gut, Clostridium can ferment carbohydrates to produce short-chain fatty acids, promoting gut health47. C. butyricum, a human gut symbiont known for its butyrate-producing and anti-cancer properties48,49, has also been isolated from soil50. However, certain Clostridium strains, including Clostridium difficile and Clostridium perfringens, produce toxins with neurotoxic, hemolytic, and enterotoxigenic properties47. They were also isolated from the soil and therefore, their transmission along the soil-plant-gut axis warrants attention51. Similarly, Acinetobacter exhibits diverse metabolic functions such as phenol and dibutyl phthalate degradation in soil, as well as phosphate solubilization for plants52,53,54. Acinetobacter species also reside in the human gut, influencing gut epithelium modulation55,56. Several Acinetobacter species, including A. baumannii and A. calcoaceticus, can be found in soil and water, but are also opportunistic human pathogens57,58. Their persistence in these different environments poses a threat to human health and may be attributed to several traits, including their high level of resistance to desiccation59, horizontal gene transfer60, and lipopolysaccharides (LPS) in their outer membrane61. Similarly, Staphylococcus and Streptococcus have been identified as opportunistic human pathogens35, but have also been detected in plant rhizospheres62,63,64,65 and soil environments66. Also, Stenotrophomonas can be considered a habitat generalist, as it inhabits both the plant rhizosphere and endosphere, where it acts as a beneficial microbe by inducing plant growth hormones and chitinases67. In soil, Stenotrophomonas plays a role in nutrient cycling, particularly in nitrogen and sulfur67. In humans, Stenotrophomonas can colonize the gut49,68 and act as a pathogen to immunocompromised and debilitated individuals, leading to severe inflammation and infection69. Its persistence in diverse environments is attributed to its metabolic versatility, ability to form biofilms, production of extracellular enzymes, and resistance to multiple stress conditions69. Also, Pseudomonas and Helicobacter can be considered as habitat generalists. Except for potential pathogenic species, other human gut commensals such as Ruminococcus, which has been identified as one of the most abundant taxa in the human gut by several global studies70,71, have also been reported in the rhizosphere of Antarctic vascular plants72. Therefore, the reservoir of microbial genera along the soil-plant-gut axis may be larger than we currently know. Considering that several competitive traits and their corresponding genes are distinctly different among species of a given genus and even among strains of a given species, comparative meta-analyses will be needed to align so-called metagenome assembled genomes (MAGs) of microbiome members along the axis to further delineate and validate the taxonomic identity and frequency of habitat generalists and cross-kingdom microbiota across these different habitats beyond the genus and species level.

Putative cross-kingdom microbiota along the soil-plant-human gut axis

The core (cross-kingdom) microbiota is traditionally defined by its taxonomic composition, but also its functional roles in relation to the host should be considered73. For instance, Bacillus subtilis, known for its considerable genome diversity, thrives in various environments (Table 1)74. Capable of forming dormant endospores in response to nutrient deprivation and environmental stresses, B. subtilis acts as an important plant growth-promoting rhizobacterium, conferring biotic and abiotic stress tolerance to plants through induced systemic resistance, biofilm formation, and lipopeptide production73,75. Moreover, B. subtilis is widely employed in bioremediation75, but is also extensively studied in humans for the production of vitamins and metabolites with anticancer and antioxidant properties, potentially influencing human longevity and reducing the risk of Parkinson’s disease76. Also, Lactobacillus represents a group of bacteria with beneficial functions for humans, plants, and soil environments. In the human gut, Lactobacillus acts as a probiotic for immune regulation, inhibiting the colonization of enteric pathogens through the production of metabolites such as organic acids, hydrogen peroxide, nitric oxide, short-chain fatty acids, and bacteriocins77. The robust metabolic capabilities of Lactobacillus also contribute to its anti-inflammatory properties78. A recent meta-analysis integrating 168,000 human gut samples globally, reported that Lactobacillus is one of the most abundant gut microbiota, representing a key taxon contributing to the variability observed in gut samples from Europe and North America49. For plants, Lactobacillus has shown growth-promoting effects and has been used as a biocontrol strains in several studies79,80. In soil environments, Lactobacillus has demonstrated the ability to remediate polluting metals81. The generalist nature of Lactobacillus may be attributed to its comprehensive genetic catalog for carbohydrate and protein modification, production of host interaction factors and bacteriocins, and stress response mechanisms82. Another noteworthy genus is Streptomyces, soil-dwelling bacteria renowned for their antibiotic production, plant growth-promoting, and biocontrol traits83. While less prevalent in the human gut, Streptomyces are gaining attention as potential probiotics due to their detoxification of mycotoxins, production of extracellular polymeric substances with anticancer properties, and synthesis of anti-inflammatory polyketides84. Other microbes, such as Lactococcus, are also identified as abundant gut commensals globally49 and have been used as probiotics for treating IBD and Type 2 diabetes85, but also exhibit plant growth-promoting effects attributed to the production of organic acids and siderophores80.

In contrast to these ‘beneficial cross-kingdom microbiota’, the pathogen Salmonella enterica manifests in various disease syndromes, with food contamination as the primary mode of transmission56,86. Studies have shown that Salmonella attaches to and colonizes plants but can even infect them, with the rate of infection contingent upon the activation of the plant immune system, sometimes resulting in plant leaf chlorosis and wilting87. Additionally, soil may serve as a reservoir for Salmonella species, as S. enterica has been found in a sandy loamy soil88. Other human pathogenic bacteria, such as the enteric pathogen Shigella, have been found to colonize the leaves and roots of Arabidopsis through the adoption of type III effectors56,89. However, the effects of Shigella on plants and its survival in soil still require further investigation. Thus, it is imperative to further explore the vast reservoir of beneficial and deleterious cross-kingdom microbial taxa along the soil-plant-human gut axis at genus and preferably at species and strain levels. In this context, identification of the extensive intraspecific diversity of microbial genera is essential to better define their specialist or generalist behavior across the soil-plant-human gut microbiome axis and to identify specific genes or gene clusters associated with that lifestyle90.

Feedback loop and co-evolution between soil, plant and human gut microbiomes

Species originating from distinct lineages can undergo reciprocal evolutionary changes over time, leading to the establishment of interdependent ecological relationships that significantly influence their phenotypes91. Co-evolution is defined as the process whereby a change in a trait of individuals within one population occurs in response to a trait exhibited by individuals in a second population92. In the context of the soil-plant-human microbiome axis, the soil acts as a reservoir for various bacterial taxa such as Helicobacter pylori, which can transfer to the human gut through food contamination or wastewater used for irrigation93,94. Nucleotide sequences of H. pylori in the environment show 96%-100% homology with those in the human gut95. The bacterium’s highly plastic genome, marked by intraspecific recombination, enhances its colonization ability in the human gut, even under antibiotic pressure96,97. In H. pylori, distinct resistance profiles, encompassing single and multidrug resistance, were identified98. Antimicrobial resistance genes induced by medical therapeutics may be reintroduced back into the soil microbiome and impose a subsequent selection pressure on soil-borne H. pylori, which in turn may augment the risk of new infections in humans99. A second example of a bacterium that may exert a reciprocal influence along the soil-plant-human gut microbiome axis includes Pseudomonas. The persistence of Pseudomonas in various habitats may be attributed to its versatile metabolic ability to utilize a wide range of organic and inorganic compounds as energy sources49,100,101, its ability to form protective biofilms to survive environmental stresses102, and the presence of multidrug efflux pumps, which contribute to its antibiotic resistance103. The combination of its genomic plasticity, environmental exposure, and biofilm formation makes horizontal gene transfer particularly prominent in Pseudomonas, enabling it to easily acquire foreign genes and disseminate antibiotic resistance genes, toxins, and other advantageous traits104, eventually mediating functional changes in the different microbiomes along the axis105.

To date, several mechanisms have been proposed that drive these reciprocal effects and co-evolution among soil, plant, and human gut microbiomes. These include molecular mimicry, horizontal gene transfer, cross-feeding, and host selection (Table 2). These mechanisms will be discussed in more detail below.

Table 2 Examples of mechanisms governing reciprocal effects along the soil-plant-gut microbiome axis
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Molecular mimicry

Molecular mimicry is characterized by analogous structural features shared by molecules originating from distinct genes or their corresponding protein products106. Microorganisms in one microbiome can produce molecules that exhibit structural similarity to essential signaling molecules in the other microbiome (Table 2). This resemblance may give rise to selection pressures between the interconnected microbiomes. For example, lipopolysaccharides (LPS) in the outer membrane of soil-borne Gram-negative bacteria have long been used as markers of soil microbial community structure107. Its structural features also resemble those of host-derived molecules that trigger pattern recognition receptors, such as Toll-like receptors (TLRs) in plants and humans108. In the human gut, this activation subsequently initiates inflammatory responses that not only contribute to tissue immunity but also facilitates coordination with the adaptive immune system109. This structural similarity can result in LPS acting as a pathogen-associated molecular pattern (PAMP), eliciting an immune response that spans plant and human systems110. Another example is peptidoglycan in the bacterial cell wall that is a direct target for innate immune receptors and modulates the accessibility of other PAMPs to additional innate immune receptors111. It has been suggested that this peptidoglycan-mediated host immunity is evolutionary conserved112. Application of eight common clinical antibiotics to soil resulted in significant alterations in gene expression, including the biosynthesis of peptidoglycan113. Hypothetically, these alterations in turn may affect human immunity via exposure to qualitative and quantitative changes in these cellular structures of soil microorganisms when transmitted to the human gut microbiome. Although most examples described so far relate to molecules of pathogenic bacteria, there are a few examples of beneficial molecular mimicry. One such as example is the soil-dwelling butyrate producer Kineothrix alysoides, whose abundance in the gut increased significantly following exposure to high-biodiversity soil10. Butyrate enhances human health by modulating energy metabolism, improving insulin sensitivity, regulating lipid metabolism, and reducing inflammation, primarily through activation of G-protein coupled receptors (GPRs) and epigenetic regulation of gene expression114. Hence, human immune responses may be modulated via the plant115 and food microbiome116, while human activities can affect the biosynthesis and dynamics of these molecules within the soil environment.

Horizontal gene transfer

Horizontal gene transfer is an extensively studied mechanism of interaction between the soil microbiome and the human gut microbiome115,117. Horizontal gene transfer represents mechanisms through which microorganisms acquire foreign DNA from other (micro)organisms. The main mechanisms of horizontal gene transfer within natural microbial communities include transformation, conjugation, transduction, and outer membrane vesicles118. The acquired DNA may confer traits that broaden the ecological niche of a microorganism, alter its interactions with the host or confer a competitive advantage over other microorganisms118. One well-studied example in the context of the soil-plant-human gut microbiome axis is the transfer of antibiotic resistance genes introduced into the soil environment through manure, biosolids, and wastewater derived from human and animal waste119, and even microplastics120. Consequently, antibiotic-resistant bacteria and antibiotic resistance genes present in the soil microbiome can transfer to clinically relevant microbial pathogens or to the human gut microbiota through various routes such as the food chain, drinking water, or environmental exposure117,121,122. During these processes, plant selection of their microbiome and the merger with the manure microbiome, known as community coalescence, have been identified as two critical factors determining the transmission of antibiotic-resistant genes123,124. Accordingly, studies have shown that individuals exposed to specific farms exhibit gut microbiomes with antibiotic resistance gene patterns similar to those found in the environmental samples from the respective farms125. For instance, about 27% of microbes transmitted from environmental soil and dust in swine farms to the human gut harbored at least one antibiotic resistance gene125. This mechanism has the potential to induce significant and rapid co-evolutionary changes across broader phylogenetic lineages of microorganisms, irrespective of their relatedness, extending beyond the confines of solely vertical transmission between the parent and its offspring126. Another group of genes that could be transferred between the soil and human gut microbiomes is the EPS biosynthetic genes. In soil microbes, these genes support various functions, including symbiosis with plants and biofilm formation127. In the human gut, EPS biosynthesis by commensal bacteria benefits the host through immune modulation, reduced gastrointestinal stress, and pathogen inhibition128. Horizontal gene transfer of EPS production genes has been found in various environments, such as food systems129 and bacterial biofilm matrices130. Therefore, it can be hypothesized that the exchange of EPS biosynthesis genes may occur between soil microbes and human gut microbes, likely leading to beneficial reciprocal effects in both habitats along the axis.

Colonization resistance

The concept of the ‘Arms Race’, commonly applied to the co-evolution between hosts and parasites, describes the reciprocal selection that drives adaptation and counter-adaptation of the interacting partners131. Colonization resistance refers to the phenomenon where commensal microorganisms of a host act as a protective barrier against the invasion, colonization, and proliferation of both pathogens and indigenous pathobionts132 (Table 2). This concept has also been employed more broadly to characterize how the resident microbiota hinders the colonization of introduced microorganisms133. In the human gut, colonization resistance becomes evident when antibiotics are used, as several pathogens and invading microbes can only effectively colonize and proliferate in this vacuum134. The mechanisms underlying colonization resistance operate through both direct and indirect means. Indirect mechanisms encompass nutrient competition135, and antagonism by gut microbes producing antimicrobial peptides, short-chain fatty acids or secondary bile acids133. Direct mechanisms of colonization resistance include the mucosal barrier136, oxygen limitation in the gut132, and host antimicrobial peptides and cytokines132. Similarly, colonization resistance in soil can be observed when introduced beneficial microbial strains fail to persist and express specific activities in situ despite demonstrating significant effects under controlled conditions in the lab or greenhouse137. Also, the invasiveness of the human-associated bacterium Escherichia coli O157:H7 in soil was inversely related to the diversity of resident soil microbial communities138. However, microbial invaders can also establish and induce changes in soil bacterial diversity139,140. The variability in the outcome of microbial invasions may be contingent with the taxonomic and functional diversity of the resident microbiome (soil, plant or human). For example, colonization resistance of the human gut is observed under homeostasis, whereas dysbiosis of the gut microbiome compromises colonization resistance132.

Cross feeding

The fourth mechanism underlying reciprocal effects between soil, plant, and human gut microbiomes involves cross-feeding (Table 2). The cooperative exchange of metabolites as energy and nutrient source among different microbial species or strains141 is largely determined by metabolic dissimilarity and complementarity142,143. Although direct cross-feeding interactions between microbiota along the soil-plant-gut axis have not been widely demonstrated and experimentally validated, shared metabolic functions across these microbiomes suggest potential indirect influences. Bacteria in particular, frequently engage in obligate metabolic mutualisms with other (micro)organisms to expand their ecological niche144. In the human gut, plant fibers containing cellulose and hemicellulose are challenging to digest, necessitating the presence of a diverse array of degrading enzymes such as glycoside hydrolases and polysaccharide lyases. These enzymes are not produced, or are produced only in limited quantities, by mammals themselves145. Interestingly, glycoside hydrolases have been found in soil, plant and human gut microbiomes, with the bacteria producing these enzymes exhibiting conserved functions across these microbiomes146. Soil microorganisms are also capable of producing vitamins, including cobalamin147. Cobalamin (vitamin B12), is crucial in the human gut and many organisms reliant on cobalamin acquisition depend on other species for its provision148. Butyrate-producing bacteria in the gut, which have various beneficial effects on human health, require cobalamin for their growth149. While the human gut does not/seldomly directly feed on soil microbes, the plant microbiome may act as an intermediary by hosting microbes that synthesize or modify essential metabolites150. Through the consumption of plant-based foods, these metabolites, including fibers and vitamins synthesized by soil bacteria, reach the human gut, where gut microbiota further metabolize them150. This interplay along the soil-plant-human gut microbiome highlights the potential for cooperative interactions and the exchange of essential resources, without the need for direct transmission of the involved microorganisms along the axis.

Host selection

Soil type can be a factor influencing the assembly of the plant microbiome; however, its impact is context-dependent. In natural ecosystems, the effects of soil type may be less pronounced compared to agricultural settings151. However, within each soil environmental context, the local proliferation of microbes is influenced by plants, as they actively recruit microbes from the soil into the rhizosphere through selection by root exudation composition, root architecture, and plant litter decomposition152. This subsequently leads to plant species-specific microbiomes, which in turn may influence human gut microbiomes. One illustrative example is the process of plant domestication, where humans transformed wild plant species into highly productive crops for human consumption. These cultivated varieties exhibit traits such as larger fruit size, higher growth rates, and altered chemistry153. Consequently, when compared to their wild relatives, crops exhibit a reduced specific root length, higher root density, altered root exudation, and root-associated microbiomes154. This was further exemplified by microbiome studies of recombinant inbred line populations of a cross between wild relatives and their domesticated crop cultivar that exhibit changes in microbiome compositions associated with specific quantitative trait loci in crop genomes155. To what extent these changes in plant chemistry and microbiome composition affect the human gut microbiome is an emerging topic of research156. A recent study revealed an association between the presence of metabolic pathways in various fruits and vegetables and homeostasis of the human gut microbiome157. This association includes pathways related to the synthesis of glutamate and biotin, as well as numerous carbohydrate-active enzymes156,157.

Microbes, derived from plants (or the diet), along with other host factors such as immune condition and genetic makeup, contribute to the formation of specific enterotypes in the human gut158,159. For example, enterotypes are characterized as Bacteroides, Prevotella, and Ruminococcus types, based on the dominant species160. This leads to functional differentiation among these enterotypes, such as the Bacteroides enterotype, which ferments carbohydrates and possesses a broad saccharolytic potential161. The Prevotella enterotype primarily degrades mucin glycoproteins, while the Ruminococcus enterotype is involved in binding mucins, transporting them, and degrading sugars in the gut161. Conversely, the specificity of enterotypes also influences the future colonization of other microbes, as they are linked to the dysbiosis status of the gut microbiome162 or the disease status of the human host163. This makes it both an important outcome and a deterministic factor in the human host’s selection of their gut microbiome.

Outlook: creating a positive feedback loop in the soil-plant-human gut axis

The reciprocal influences as well as the distribution and proliferation of microbes along the soil-plant-gut axis are subject to various environmental factors. These factors may range from unpredictable climate change events to physiochemical changes in specific micro-habitats. Therefore, managing potential external drivers to create a positive feedback loop along the axis is essential for achieving better “One Health” outcomes.

A healthy plant microbiome can positively influence the human gut microbiome primarily through two mechanisms (Fig. 2). First, the plant phyllosphere and other edible plant parts can transmit soil microorganisms to the human gut. With increased soil microbial diversity, the potential negative impact on the gut microbiome through the plant microbiome may decrease. For instance, enhanced soil microbial diversity correlates with a decreased abundance of antibiotic-resistant genes in the soil164,165,166 and increased antagonistic effects against human pathogens167. Additionally, plant extracts, including phenolic compounds, chlorophyll, and carotenoids, can act as prebiotics for beneficial microbes already present in the human gut168. Secondly, an improved soil microbiome can sustain plants producing food with higher nutrient contents, such as vitamins, polyphenols, and dietary fiber169. For example, biofertilizers have been found to increase the dietary fiber content of onions170 and corn171, the vitamin content of tomatoes172, and the polyphenol content of eggplants173. Subsequently, this higher dietary fiber content enhances the production of short-chain fatty acids by gut bacteria, indirectly contributing to improvement in human health by reducing inflammation, preventing cancer, and supplying energy174. Furthermore, the polyphenols in food promote beneficial strains in the gut, such as A. muciniphila175 and enhance antimicrobial activities against pathogens176.

Fig. 2: Potential future steps to create positive feedback loops along the soil-plant-human gut axis.
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External drivers, such as crop rotation, diversification, cover cropping, organic compost, and ecological restoration, have been proposed to enhance soil biodiversity and health. A healthy soil ecosystem promotes nutrient uptake and enhances plant disease resistance by fostering the enrichment of beneficial microbes in the plant rhizosphere, phyllosphere and spermosphere. This, in turn, contributes to a robust plant microbiome capable of producing nutrient-rich food, including dietary fiber, polyphenols, and vitamins. The enhanced plant microbiome also has the potential to support microorganisms with probiotic effects while reducing the frequency of human pathogens and antibiotic resistance genes when transferred to the human gut. Furthermore, the soil microbiome can directly interact with the human microbiome. Moreover, a healthy human gut microbiome plays a role in decreasing the frequency of (opportunistic) human pathogens and antibiotic resistance genes reintroduced into the soil through fecal and waste matter, thus completing a positive feedback loop that benefits both soil and human health. Created in BioRender. Ma, H. (2025) https://BioRender.com/b51e6if.

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In addition to using plants as a mediator, numerous studies have demonstrated a positive link between soil biodiversity and human health, often referred to as ‘natural immunity’177,178. Particularly in early life, exposure of humans to the natural soil environment aids in the development of a diverse molecular memory, facilitating rapid recognition of harmful organisms179. Furthermore, exposure to the natural environment can introduce beneficial gut microbiota, including butyrate-producing bacteria180 and beneficial fungi181. These microbial components acquired by the gut contribute to activation of the innate immune system. For instance, feeding a soil slurry to mice has been shown to alleviate inflammation178, while exposing inbred laboratory mice to the outdoor environment reduces pathogen infections, increases circulating granulocytes, and promotes differentiation of T cell populations via the colonization of intestinal fungi181. Moreover, higher environmental biodiversity has been associated with an increased proportion of regulatory T cells and elevated plasma TGF-β1 levels in children182. Therefore, exposure to the natural environment can serve as a prophylactic measure in preventing immune-mediated diseases (Fig. 2). In return, a healthy gut microbiome may reduce the presence of antibiotic-resistant genes and human pathogens that could be reintroduced back to the soil environment through feces and waste. Thus, while exposure to the natural environment carries the risk of closer contact with potential human pathogens, a healthy soil microbiome could diminish these chances. In this way, the positive loop along the soil-plant-human gut axis can be reinforced.

Conclusions

The importance of including the soil and plant microbiomes in human health is increasingly recognized3. In this perspective, we have provided several examples of microorganisms that can transmit from soil or plants to the human gut and exert specific influences. Typical examples highlighted and detailed in the sections above include Bacillus, Pseudomonas and Clostridium species. The question if there are unifying beneficial or detrimental functions in these distinct ecosystems was more difficult to address and the available data and results are still largely circumstantial and hypothetical. To this end, we propose to integrate co-evolutionary concepts, where the soil, plant, and human gut microbiomes may influence each other’s evolutionary trajectories over time, providing a better understanding of the exchange and interactions between the soil microbiome and human gut microbiome. Also identifying habitat specialists, habitat generalists, and potential cross-kingdom microbiota along the soil-plant-human gut microbiome axis at the species and preferably strain level could provide us with a deeper understanding of the microbial fluxes along the axis. In this context, large-scale genomic identification of the extensive intraspecific diversity of microbial genera is essential to identify their life-style associated genes90 and monitor their population dynamics and distribution across the soil-plant-human gut microbiome axis.