Priority effects in microbiome assembly

Debray, Reena; Herbert, Robin A.; Jaffe, Alexander L.; Crits-Christoph, Alexander; Power, Mary E.; Koskella, Britt

doi:10.1038/s41579-021-00604-w

Cited by 264 publications

(201 citation statements)

References 139 publications

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“…While by design, causality cannot be inferred from our data, these results tie in with existing ecological theories on microbiome stability and resilience, e.g. on tipping elements and critical transitions 45,46 , community multi-stability leading to enterotypes 47,48 , priority 49 or Anna Karenina effects 50 . We found limited evidence for colonisation facilitation across species boundaries, both in donor and recipient.…”

Section: Both Neutral and Adaptive Processes Shape Post-fmt Strain Population Dynamicssupporting

confidence: 84%

Drivers and Determinants of Strain Dynamics Following Faecal Microbiota Transplantation

Schmidt¹,

Maistrenko³

et al. 2021

Preprint

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Faecal microbiota transplantation (FMT) is an efficacious therapeutic intervention, but its clinical mode of action and underlying microbiome dynamics remain poorly understood. Here, we analysed the metagenomes associated with 142 FMTs, in a time series-based meta-study across five disease indications. We quantified strain-level dynamics of 1,089 microbial species based on their pangenome, complemented with 47,548 newly constructed metagenome-assembled genomes. Using subsets of procedural-, host- and microbiome-based variables, LASSO-regularised regression models accurately predicted the colonisation and resilience of donor and recipient microbes, as well as turnover of individual species. Linking this to putative ecological mechanisms, we found these sets of variables to be informative of the underlying processes that shape the post-FMT gut microbiome. Recipient factors and complementarity of donor and recipient microbiomes, encompassing entire communities to individual strains, were the main determinants of individual strain population dynamics, and mostly independent of clinical outcomes. Recipient community state and the degree of residual strain depletion provided a neutral baseline for donor strain colonisation success, in addition to inhibitive priority effects between species and conspecific strains, as well as putatively adaptive processes. Our results suggest promising tunable parameters to enhance donor flora colonisation or recipient flora displacement in clinical practice, towards the development of more targeted and personalised therapies.

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Section: Both Neutral and Adaptive Processes Shape Post-fmt Strain Population Dynamicssupporting

confidence: 84%

Drivers and Determinants of Strain Dynamics Following Faecal Microbiota Transplantation

Schmidt¹,

Maistrenko³

et al. 2021

Preprint

View full text Add to dashboard Cite

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“…Such knowledge is critical to control (e.g., maintain ecosystem services), promote (e.g., bioinoculants for higher agricultural productivity) and avoid (e.g., pytopathogens) colonisation by alien microbes (species not currently part of resident microflora). Recently, the priority effect, which refers to that early incoming microbes may outcompete late arrivals by numerical and prior adaptation advantages, is proposed to address this issue 18,19 . For example, microbial competition in wheat roots revealed a significant advantage of an early incoming coloniser, a seed endophyte Pantoea agglomerans , over late‐incoming colonisers 20 .…”

Section: Introductionmentioning

confidence: 99%

“…Recently, the priority effect, which refers to that early incoming microbes may outcompete late arrivals by numerical and prior adaptation advantages, is proposed to address this issue. 18,19 For example, microbial competition in wheat roots revealed a significant advantage of an early incoming coloniser, a seed endophyte Pantoea agglomerans, over late-incoming colonisers. 20 However, measuring the persistence of microbial inoculants in natural soils is challenging because of the confounding influence of the complex diversity of native soil microbes.…”

mentioning

confidence: 99%

Effective colonisation by a bacterial synthetic community promotes plant growth and alters soil microbial community

Liu

Qiu

et al. 2021

J of Sust Agri & Env

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Introduction Plant‐associated microorganisms are widely explored for their use as bioinoculants in agriculture. However, the rate and ability of introduced microbes to colonise and interact with indigenous soil microbiomes are largely unknown. Materials & Methods In this study, we constructed a bacterial synthetic community (SynCom) using eight plant‐growth‐promoting bacteria isolated from the wheat (Triticum aestivum) rhizosphere, including three Bacillus spp., two Acinebacter spp., an Enterobacter sp., a Xanthomonas sp. and a Burkholderia sp., which all showed multiple plant growth‐promoting effects including indole‐3‐acetic acid and ammonia production and fungal pathogen suppression. We inoculated this SynCom in a soil with reduced microbial diversity, and investigated the ability of the SynCom to colonise wheat plants, and interact with soil microbes in the presence or absence of a soil‐borne pathogen Fusarium pseudograminearum (Fp). Results We found that SynCom significantly increased the wheat plant growth, root development and biomass production. Fp load in soil was significantly reduced and plant survival rates increased following the SynCom inoculation. Soil microbial community structure was altered by the SynCom, and noticeably, relative abundance of Pseudomonas spp. was induced in the soil. Conclusion This study provides novel evidence that colonisation of a beneficial SynCom promotes plant growth and alters soil microbial community.

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“…This is expected if early-arriving species improve the environment, facilitating the growth of others that are less well adapted to it (38–41). Alternative dynamics are possible if the first colonizers alter the environment in a way that strongly inhibits future invaders (31), or if late colonizers out-compete earlier ones and replace them (56), but this is not what we observe in our system.…”

Section: Discussionmentioning

confidence: 60%

“…As time passes, resident species may co-evolve to reduce niche overlap and availability in a way that would prevent further invasion. The Community Monopolization Hypothesis predicts that early colonisers adapt to use available resources efficiently, yielding a competitive advantage against later-arriving species (49–52), also known as a “priority effect” (31, 53). One may also expect such co-evolved resident species to be less perturbed by species invasion (49).…”

Section: Introductionmentioning

confidence: 99%

Microbial invasion of a toxic medium is facilitated by a resident community but inhibited as the community co-evolves

Piccardi

Alberti

Alexander

et al. 2022

Preprint

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Predicting whether microbial invaders will colonize an environment is critical for managing natural and engineered ecosystems, and controlling infectious disease. Invaders often face competition by resident microbes. But how invasions play out in communities dominated by facilitative interactions is less clear. We previously showed that growth medium toxicity can promote facilitation between four bacterial species, as species that cannot grow alone rely on others to survive. Following the same logic, here we allowed other bacterial species to invade the four-species community, and found that invaders could more easily colonize a toxic medium when the community was present. In a more benign environment instead, invasive species that could survive alone colonized more successfully when the residents were absent. Next, we asked whether early colonists could exclude future ones through a priority effect, by inoculating the invaders into the resident community only after its members had co-evolved for 44 weeks. Compared to the ancestral community, the co-evolved resident community was more competitive toward invaders, and less affected by them. Our experiments show how communities may assemble by facilitating one another in harsh, sterile environments, but that arriving after community members have co-evolved can limit invasion success.

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Priority effects in microbiome assembly

Cited by 264 publications

References 139 publications

Drivers and Determinants of Strain Dynamics Following Faecal Microbiota Transplantation

Drivers and Determinants of Strain Dynamics Following Faecal Microbiota Transplantation

Effective colonisation by a bacterial synthetic community promotes plant growth and alters soil microbial community

Microbial invasion of a toxic medium is facilitated by a resident community but inhibited as the community co-evolves

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