One Health and the role of the microbiome

Traditionally, clinical microbiology focused on the role of individual microbes in human and animal disease. That has changed in recent decades. We now know that the health and wellbeing of humans depends on entire communities of microbes that exist in our bodies. We are still figuring out how deep that connection goes.

Even more recently, the thinking around microbiome research has taken a step further. Welcome to the “One Health” concept. This term refers to ecological relationships between humans, animals, and the environment – in particular, how the health of one can impact the others.

The One Health concept itself is not a new one. The term was first mentioned in 2004, when the Wildlife Conservation Society organised a conference with the theme “One World, One Health”. At this conference, the Manhattan Principles were formulated, a list of recommendations for taking a holistic approach to maintaining ecosystem integrity and preventing threats to human and animal health. At the time, this was in relation to the prevention of epidemic diseases.

The connection between microbiomes

In the context of the microbiome, the One Health concept refers to the idea that the microbial communities living within and on different organisms, as well as in the environment, are interconnected, forming a global ecosystem^[1].

In other words, no microbiome is an island.

Why does this matter? It highlights the importance of a holistic approach to the microbiome, that recognises the various influences that the microbiome of an individual or environment may have. This is multidirectional: human activities can shape human, animal, and environmental microbiomes and in turn, changes in these microbiomes can impact human health.

For example, changes in the environmental microbiome (e.g., due to urbanization) could affect the composition of the human skin or gut microbiome, in turn influencing the incidence of diseases in humans. We can also see the influence of animal microbiomes on the human microbiome. For example, pet ownership has been associated with greater skin microbiome diversity, and studies have shown that co-habiting family members share microbial communities with each other and their dogs^[2]. There is even a suggestion that exposure to animals at an early age reduces a child’s risk of developing asthma^[3], although this link needs to be investigated further.

Antibiotic resistance

One example of where the One Health concept is important in microbiome research is the development of antibiotic resistance^[4]. Bacteria can develop antibiotic resistance through natural selection, but they can also acquire this trait from other bacteria. This is because bacteria can share genetic material by a mechanism called horizontal gene transfer. If one bacterium within a microbiome develops antibiotic resistance, it can in principle share this with other bacteria in that community. In this way, microbiomes can act as a reservoir for antibiotic resistance genes and – crucially – these genes can in principle transfer between different microbiomes. To combat the issue of antibiotic resistance, it is essential to appreciate this dynamic and implement responsible use of antibiotics in healthcare, agricultural and veterinary settings.

The soil microbiome

Another fascinating area of research is the effect the soil microbiome has on human and animal health. Soil is the largest reservoir of microbial diversity on Earth, with an estimated >50,000 species of microbes per gram – this makes the soil a major source of microorganisms and thus a foundation of One Health^[5]. The soil microbiome contributes to the diversity of animal gut microbiomes – it has been estimated that up to 3% of the rumen microbiome of sheep and cattle originates from ingested soil^[6].

Certain animals deliberately consume soil, which is referred to as “geophagy”, and there is evidence to suggest that this sort of behaviour has health benefits. For example, soil-dwelling mice directly acquire microorganisms from the soil that can alleviate inflammation and allergic diseases^[7]. There is even evidence that microorganisms obtained in this way can reduce anxiety, suggesting a link with the gut-brain axis^[8]. Indeed, microorganisms from the soil can also be passed on to dog and cat owners via their pets, highlighting the interconnectivity between the soil, animal, and human microbiomes^[9].

Interestingly, the flow of information goes in both directions. For example, cattle can pass on antibiotic resistance genes from the rumen microbiome to the soil^[10] - which is important to appreciate when tackling the issue of antibiotic resistance.

Microorganisms in the soil also play a fundamental role in delivering nutrients to plants and thus the soil microbiome is intimately linked with the plant health. “Disease suppressive soils” (which contain microorganisms that contribute to disease resistance in plants) play a vital role in conferring plant resistance to pathogens^[11]. This system hangs in the balance – global increases in temperature may increase plant disease by altering the abundance of soil-borne pathogens.

Considerations for the future

It is clear that the interactions between microbiomes will need to be considered when tackling global issues such as disease and climate change. What is perhaps less clear is whether interventions are possible (and if so, what form this would take). For example, one review article suggests that we could assess and modify the microbiomes of our immediate surroundings (or even our pets), to enhance the health of humans and animals in the household or workplace^[12]. The authors acknowledge that this is very speculative at this point, but it will be interesting to see how the field develops from here.

References

1. Trinh et al. (2018)
2. Song et al. (2013)
3. Jhun and Phipatanakul (2016)
4. Aslam et al. (2021)
5. Banerjee and van der Heijden (2023)
6. Attwood (2019)
7. Ottman et al. (2019)
8. Liddicoat et al. (2020)
9. Ross et al. (2018)
10. Hui-Zeng Sun et al. (2021)
11. Banerjee and van der Heijden (2023)
12. Trinh et al. (2018)