Microbial cross-feeding promotes multiple stable states and species coexistence, but also susceptibility to cheaters

Sun, Zepeng; Koffel, Thomas; Stump, Simon Maccracken; Grimaud, Ghjuvan Micaelu; Klausmeier, Christopher A.

doi:10.1016/j.jtbi.2019.01.009

Cited by 26 publications

(36 citation statements)

References 61 publications

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“…We modeled the substrate as a nutrient, but it can also be interpreted as the limited availability of space 26 . In fact, the obtained phase plane and the nullclines, describing the dynamics of the species, are observed in different mutualistic models [20][21][22][23]46 , so that we can state this is a general phenomenon. Therefore, our results give insights into necessary conditions for obligate mutualistic models: there needs to be an Allee effect as well as a limiting function.…”

Section: /15mentioning

confidence: 82%

“…Another disadvantage of the existence of a survival threshold is that it creates susceptibility to cheaters 23 . A cheater is an individual of the species which does not cooperate in the creation of cross-feeding nutrients, thereby creating an energetic advantage over the cooperators and potentially increasing the risk of a collapse of the system 41 .…”

Section: /15mentioning

confidence: 99%

“…A density threshold between two different states of the system, in this case survival and extinction, is related to the concept of bistability. Different models have shown that mutualism can cause bistability via the interdependence between the species [20][21][22][23] . In some of these models the species are competitive as well as mutualistic, e.g.…”

Section: Introductionmentioning

confidence: 99%

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Mutualistic cross-feeding in microbial systems generates bistability via an Allee effect

Gonze

Gelens

Vet

2019

Preprint

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ABSTRACTMutualistic interactions are characterized by the positive influence that two species exert on each other. Such mutualism can lead to bistability. Depending on the initial population size species will either survive or go extinct. Various phenomenological models have been suggested to describe bistability in mutualistic systems. However, these models do not account for interaction mediators such as nutrients. In contrast, nutrient-explicit models do not provide an intuitive understanding of what causes bistability. Here, we reduce a theoretical nutrient-explicit model of two mutualistic cross-feeders in a chemostat, uncovering an explicit relation to a growth model with an Allee effect. We show that the dilution rate in the chemostat leads to bistability by turning a weak Allee effect into a strong Allee effect. This happens as long as there is more production than consumption of cross-fed nutrients. Thanks to the explicit relationship of the reduced model with the underlying experimental parameters, these results allow to predict the biological conditions that sustain or prevent the survival of mutualistic species.

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Section: /15mentioning

confidence: 82%

Section: /15mentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Mutualistic cross-feeding in microbial systems generates bistability via an Allee effect

Gonze

Gelens

Vet

2019

Preprint

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“…Second, cooperative, complementary (labor-divided) microbial metabolic interaction networks might be unstable and prone to collapse due to cheaters. Theoretical models have demonstrated that exploiters (partial secretors with a reduced genotype) actually cheat on full secretors [132,133]. It was found that the loss of a gene from a full secretor meant that the external product concentration (and thus overall group growth) is decreased, contrary to how the Black Queen hypothesis suggests the emergence of streamlined cooperative genotypes.…”

Section: Issues Of Syntrophic Consortiamentioning

confidence: 99%

Endosymbiosis before eukaryotes: mitochondrial establishment in protoeukaryotes

Zachar

Boza

2020

Cell. Mol. Life Sci.

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Endosymbiosis and organellogenesis are virtually unknown among prokaryotes. The single presumed example is the endosymbiogenetic origin of mitochondria, which is hidden behind the event horizon of the last eukaryotic common ancestor. While eukaryotes are monophyletic, it is unlikely that during billions of years, there were no other prokaryote-prokaryote endosymbioses as symbiosis is extremely common among prokaryotes, e.g., in biofilms. Therefore, it is even more precarious to draw conclusions about potentially existing (or once existing) prokaryotic endosymbioses based on a single example.It is yet unknown if the bacterial endosymbiont was captured by a prokaryote or by a (proto-)eukaryote, and if the process of internalization was parasitic infection, slow engulfment, or phagocytosis. In this review, we accordingly explore multiple mechanisms and processes that could drive the evolution of unicellular microbial symbioses with a special attention to prokaryote-prokaryote interactions and to the mitochondrion, possibly the single prokaryotic endosymbiosis that turned out to be a major evolutionary transition. We investigate the ecology and evolutionary stability of inter-species microbial interactions based on dependence, physical proximity, cost-benefit budget, and the types of benefits, investments, and controls. We identify challenges that had to be conquered for the mitochondrial host to establish a stable eukaryotic lineage. Any assumption about the initial interaction of the mitochondrial ancestor and its contemporary host based solely on their modern relationship is rather perilous. As a result, we warn against assuming an initial mutually beneficial interaction based on modern mitochondria-host cooperation. This assumption is twice fallacious: (i) endosymbioses are known to evolve from exploitative interactions and (ii) cooperativity does not necessarily lead to stable mutualism. We point out that the lack of evidence so far on the evolution of endosymbiosis from mutual syntrophy supports the idea that mitochondria emerged from an exploitative (parasitic or phagotrophic) interaction rather than from syntrophy.Publisher's Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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“…70 However, recent theoretical models have found that cross-feeding can dramatically increase the 71 diversity of taxa, even in a homogenous environment [6, 10,12]. Furthermore, multiple different 72 types of models have found that introducing cross-feeding into communities can result in a new 73 stable community composition [13][14][15]. However, fewer studies have examined how the strength 74 of cross-feeding relationships alters other emergent properties, such as susceptibility to invasion.…”

Section: Introduction 35mentioning

confidence: 99%

Disruption of cross-feeding interactions by invading taxa can cause invasional meltdown in microbial communities

Herren

2020

Preprint

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AbstractThe strength of biotic interactions within an ecological community affects the susceptibility of the community to invasion by introduced taxa. In microbial communities, cross-feeding is a widespread type of biotic interaction that has the potential to affect community assembly and stability. Yet, there is little understanding of how the presence of cross-feeding within a community affects invasion risk. Here, I develop a metabolite-explicit model where native microbial taxa interact through both cross-feeding and competition for metabolites. I use this model to study how the strength of biotic interactions, especially cross-feeding, influence whether an introduced taxon can join the community. I found that stronger cross-feeding and competition led to much lower invasion risk, as both types of biotic interactions lead to greater metabolite scarcity for the invader. I also evaluated the impact of a successful invader on community composition and structure. The effect of invaders on the native community was greatest at intermediate levels of cross-feeding; at this “critical” level of cross-feeding, successful invaders generally causing decreased diversity, decreased productivity, greater metabolite availability, and decreased quantities of metabolites exchanged among taxa. Furthermore, these changes resulting from a successful primary invader made communities further susceptible to future invaders. The increase in invasion risk was greatest when the network of metabolite exchange between taxa was minimally redundant. Thus, this model demonstrates a case of invasional meltdown that is mediated by initial invaders disrupting the metabolite exchange networks of the native community.

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Microbial cross-feeding promotes multiple stable states and species coexistence, but also susceptibility to cheaters

Cited by 26 publications

References 61 publications

Mutualistic cross-feeding in microbial systems generates bistability via an Allee effect

Mutualistic cross-feeding in microbial systems generates bistability via an Allee effect

Endosymbiosis before eukaryotes: mitochondrial establishment in protoeukaryotes

Disruption of cross-feeding interactions by invading taxa can cause invasional meltdown in microbial communities

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