Microbiome: Finding common connections
Living inside the gut of most mammals, including humans, is a unique cocktail of bacteria and other microbes collectively known as the gut microbiome. How individuals end up hosting such varied populations depends not only on the microbes they acquire from their environment, but also on how these organisms ecologically interact with one another inside the gut. For example, some microbes may be excluded from a host by a competitor (negative association; Mäklin et al., 2022), while others may be promoted to grow due to the mutual benefits provided by another microbe (positive association; Seth and Taga, 2014). Which bacteria end up in the microbiome has consequences for the health of the host (Suzuki, 2017). Therefore, understanding how bacteria in the gut interact, and whether these interactions are consistent across individuals, could help researchers develop better therapeutic drugs for recovering and maintaining a healthy gut microbiome.
Negative and positive interactions are typically measured by growing closely related groups of bacteria, known as taxa, in the presence or absence of other taxa (Foster and Bell, 2012; Gould et al., 2018). However, these kinds of experiments are practically impossible to carry out for communities as diverse as the gut microbiome. To overcome this, scientists study individual microbiomes to determine which bacterial taxa frequently occur together (suggesting they promote each other’s growth), and which rarely inhabit the same host (suggesting they are likely to be competitors). However, this approach does not reveal if interactions are consistent across different hosts (i.e. universal), or are unique to bacterial communities inside each individual.
Now, in eLife, Elizabeth Archie from the University of Notre Dame and colleagues – including Kimberley Roche as first author – report how different bacterial taxa fluctuate over time in the gut of wild baboons to determine if the interactions between them are universal (Roche et al., 2023). The team (who are based at various institutes in the United States and Germany) used data from a long-term study of wild baboons living in Amboseli, Kenya which had their microbiomes sampled hundreds of times between 2000 and 2013. Using a statistical model they had developed, Roche et al. tracked how the quantity of individual taxa rose and declined over time. These traces were then compared to determine which bacterial taxa fluctuated together (positive association) and which rose and fell in opposing directions (negative association).
Next, Roche et al. examined if the associations among bacteria were comparable across individuals. The strength and direction of the correlations (i.e. whether they were positive or negative) were remarkably consistent across the 56 baboons studied, suggesting that ecological interactions in the gut microbiome are mostly universal (Figure 1). Most of these associations were relatively weak and negative, suggesting that gut bacteria usually do not help one another grow, but rather compete with each other or thrive in different states, such as hosts with specific variations in their immune or endocrine systems. This result aligns well with ecological theory which predicts that strong, positive dependencies within a community should be rare, as highly interdependent ecosystems are likely to be unstable (Coyte et al., 2015) – a phenomenon Roche et al. refer to as an ‘ecological house of cards’.
It is unclear how many of these universal associations arise from direct ecological interactions between microbes, and how many arise from bacterial taxa simply preferring similar or different host environments. Roche et al. make a compelling case that both of these processes might be at play. They show that environmental similarity (e.g. diet) between hosts does not influence universality scores, supporting the idea that these associations reflect true ecological interactions. Furthermore, they show that associations with the highest universality score were positive relationships between closely related bacteria, suggesting that these interactions may be partly due to bacteria responding to a host’s internal state or environment in a similar way.
These findings suggest that while the composition of microbes in the gut can be highly individualised, the underlying ecology shaping this variation may be similar. This is good news for scientists developing therapies to modify the gut microbiome, such as probiotics, since it means that different microbiomes are likely to react predictably to interventions. Moreover, the ability to infer ecological phenomena from microbiome data has tremendous value for ecology as a whole.
The last century has seen a vast number of mathematical models for describing ecological theories, such as the theory of ecological succession (Cowles, 1899). However, testing these models in large-scale ecosystems is challenging as it usually requires data that has been collected over long periods of time, such as seeing a forest grow from its initial state to a stable climax. The findings of Roche et al. suggest that many hypotheses of ecological theory could instead be tested with data from microbiomes – which vary greatly across space, change quickly, but follow the same ecological principles as the large-scale ecological world we perceive. This new approach could bring scientists one step closer to answering many unexplored questions in ecology which, ultimately, govern our ability to survive on this planet.
References
-
Microbiome interactions shape host fitnessPNAS 115:E11951–E11960.https://doi.org/10.1073/pnas.1809349115
-
Strong pathogen competition in neonatal gut colonisationNature Communications 13:7417.https://doi.org/10.1038/s41467-022-35178-5
-
Nutrient cross-feeding in the microbial worldFrontiers in Microbiology 5:350.https://doi.org/10.3389/fmicb.2014.00350
-
Links between natural variation in the microbiome and host fitness in wild mammalsIntegrative and Comparative Biology 57:756–769.https://doi.org/10.1093/icb/icx104
Article and author information
Author details
Publication history
Copyright
© 2023, Santiago and Raulo
This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 437
- views
-
- 23
- downloads
-
- 0
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Ecology
- Microbiology and Infectious Disease
Interspecies interactions involving direct competition via bacteriocin production play a vital role in shaping ecological dynamics within microbial ecosystems. For instance, the ribosomally produced siderophore bacteriocins, known as class IIb microcins, affect the colonization of host-associated pathogenic Enterobacteriaceae species. Notably, to date, only five of these antimicrobials have been identified, all derived from specific Escherichia coli and Klebsiella pneumoniae strains. We hypothesized that class IIb microcin production extends beyond these specific compounds and organisms. With a customized informatics-driven approach, screening bacterial genomes in public databases with BLAST and manual curation, we have discovered 12 previously unknown class IIb microcins in seven additional Enterobacteriaceae species, encompassing phytopathogens and environmental isolates. We introduce three novel clades of microcins (MccW, MccX, and MccZ), while also identifying eight new variants of the five known class IIb microcins. To validate their antimicrobial potential, we heterologously expressed these microcins in E. coli and demonstrated efficacy against a variety of bacterial isolates, including plant pathogens from the genera Brenneria, Gibbsiella, and Rahnella. Two newly discovered microcins exhibit activity against Gram-negative ESKAPE pathogens, i.e., Acinetobacter baumannii or Pseudomonas aeruginosa, providing the first evidence that class IIb microcins can target bacteria outside of the Enterobacteriaceae family. This study underscores that class IIb microcin genes are more prevalent in the microbial world than previously recognized and that synthetic hybrid microcins can be a viable tool to target clinically relevant drug-resistant pathogens. Our findings hold significant promise for the development of innovative engineered live biotherapeutic products tailored to combat these resilient bacteria.
-
- Ecology
For the first time in any animal, we show that nocturnal bull ants use the exceedingly dim polarisation pattern produced by the moon for overnight navigation. The sun or moon can provide directional information via their position; however, they can often be obstructed by clouds, canopy, or the horizon. Despite being hidden, these bodies can still provide compass information through the polarised light pattern they produce/reflect. Sunlight produces polarised light patterns across the overhead sky as it enters the atmosphere, and solar polarised light is a well-known compass cue for navigating animals. Moonlight produces an analogous pattern, albeit a million times dimmer than sunlight. Here, we show evidence that polarised moonlight forms part of the celestial compass of navigating nocturnal ants. Nocturnal bull ants leave their nest at twilight and rely heavily on the overhead solar polarisation pattern to navigate. Yet many foragers return home overnight when the sun cannot guide them. We demonstrate that these bull ants use polarised moonlight to navigate home during the night, by rotating the overhead polarisation pattern above homing ants, who alter their headings in response. Furthermore, these ants can detect this cue throughout the lunar month, even under crescent moons, when polarised light levels are at their lowest. Finally, we show the long-term incorporation of this moonlight pattern into the ants’ path integration system throughout the night for homing, as polarised sunlight is incorporated throughout the day.