Host-initiated microbial association leads to stable ectosymbiosis in an ecological model
5 affiliations
- 1Institute of Evolution, HUN-REN Centre for Ecological Research, Budapest, Hungary
- 2Doctoral School of Biology, Institute of Biology, Eötvös Loránd University, Budapest, Hungary
- 3Department of Plant Systematics, Ecology and Theoretical Biology, Institute of Biology, Eötvös Loránd University, Budapest, Hungary
- 4Parmenides Center for the Conceptual Foundations of Science, Parmenides Foundation, Pöcking, Germany
- 5Chair for Computational and Theoretical Biology, Julius-Maximilians University, Würzburg, Germany
Abstract
Microbial symbiosis is widespread among metabolically coupled cells; it presumably gave rise to mitochondria. However, how such symbioses emerge, evolve, and stabilize are unknown, particularly in the prokaryotic domain where endosymbiosis is virtually nonexistent. Yet there is growing evidence suggesting that mitochondria originated from such a metabolically driven prokaryotic partnership rather than phagocytotic predation. While prokaryotes almost ubiquitously engage in metabolic syntrophy, it is unknown whether syntrophy alone can enable stable physical associations that could pave the road toward physical integration. Here, we tested the hypothesis that syntrophy can transition into stable ectosymbiosis, using an ecological mathematical model. Starting from an existing syntrophic partnership between free-living hosts and symbionts, we demonstrate that population-level obligate ectosymbiosis can emerge and stabilize, even in unilateral syntrophy where only the symbiont consumes a host-produced metabolite. A key assumption is that the hosts’ by-product inhibits their growth when it accumulates. By consuming the toxic by-product, the symbiont locally reduces hosts’ self-inhibition at the contact surface, manifesting as a private benefit providing selective advantage. Our results show that due to the direct and indirect benefits, the ectosymbiotic consortium is stable against free-living forms and the consortial cooperation is ecologically selected for. Furthermore, solid metabolic coupling promotes population-level obligacy, ultimately excluding free-living individuals under stricter conditions. Our results support the hypothesis that cooperative, syntrophic microbes (particularly prokaryotes) are capable of forming stable, physical, and species-specific ectosymbiosis through inhibition reduction, providing a plausible first step toward potential, gradual endosymbiotic integration. Our work bridges the gap between models of microbial cooperation between free-living species and models that assume already-concluded, fully integrated endosymbiosis under multilevel selection. Author summary: Metabolic interactions among microbes are integral to their associations ranging from cross-feeding between free-living individuals to physically integrated cells. While metabolic coupling among free-living microbes is ubiquitous, the conditions that enable and facilitate a more intimate physical connection or even integration remain unclear. This is mostly because we do not know examples that demonstrate how the process unfolds and we lack intermediates of the most important and perhaps the first of such integrations: mitochondria. With the potential benefits of forming a higher unit of selection by prolonged association, we hypothesize that an evolutionary path could exist from free-living syntrophic partners toward obligate endosymbiosis through the intermediate stage of syntrophic ectosymbiosis. Here we provide a theoretical model that demonstrates that host-initiated ectosymbiosis can be stable, even when the cross-feeding with the bound symbionts is unilateral. Our results demonstrate that the physical association with a syntrophic partner is selected for as a mechanism to survive a self-produced toxic metabolite. Self-inhibition turns out to be crucial as the feeding symbiont reducing it effectively provides the necessary benefit for the host. Our model provides a potential mechanism of an ecological driver that could hypothetically lead to the endosymbiotic origin of mitochondria among prokaryotic partners (alphaproteobacterium and Asgard archaeon), without assuming a direct metabolic benefit for the host.
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BibTeX
@article{krishnan2026hostinitiated,
title = {{Host-initiated microbial association leads to stable ectosymbiosis in an ecological model}},
author = {Nandakishor Krishnan and István Zachar and Ádám Kun and Chaitanya S. Gokhale and József Garay},
journal = {PLOS Computational Biology},
year = {2026},
month = sep,
doi = {10.1371/journal.pcbi.1014699},
url = {https://journals.plos.org/ploscompbiol/article?id=10.1371/journal.pcbi.1014699},
note = {CC BY 4.0},
}
RIS
TY - JOUR
TI - Host-initiated microbial association leads to stable ectosymbiosis in an ecological model
AU - Nandakishor Krishnan
AU - István Zachar
AU - Ádám Kun
AU - Chaitanya S. Gokhale
AU - József Garay
PY - 2026
DA - 2026/09/02
JO - PLOS Computational Biology
DO - 10.1371/journal.pcbi.1014699
UR - https://journals.plos.org/ploscompbiol/article?id=10.1371/journal.pcbi.1014699
AB - Microbial symbiosis is widespread among metabolically coupled cells; it presumably gave rise to mitochondria. However, how such symbioses emerge, evolve, and stabilize are unknown, particularly in the prokaryotic domain where endosymbiosis is virtually nonexistent. Yet there is growing evidence suggesting that mitochondria originated from such a metabolically driven prokaryotic partnership rather than phagocytotic predation. While prokaryotes almost ubiquitously engage in metabolic syntrophy, it is unknown whether syntrophy alone can enable stable physical associations that could pave the road toward physical integration. Here, we tested the hypothesis that syntrophy can transition into stable ectosymbiosis, using an ecological mathematical model. Starting from an existing syntrophic partnership between free-living hosts and symbionts, we demonstrate that population-level obligate ectosymbiosis can emerge and stabilize, even in unilateral syntrophy where only the symbiont consumes a host-produced metabolite. A key assumption is that the hosts’ by-product inhibits their growth when it accumulates. By consuming the toxic by-product, the symbiont locally reduces hosts’ self-inhibition at the contact surface, manifesting as a private benefit providing selective advantage. Our results show that due to the direct and indirect benefits, the ectosymbiotic consortium is stable against free-living forms and the consortial cooperation is ecologically selected for. Furthermore, solid metabolic coupling promotes population-level obligacy, ultimately excluding free-living individuals under stricter conditions. Our results support the hypothesis that cooperative, syntrophic microbes (particularly prokaryotes) are capable of forming stable, physical, and species-specific ectosymbiosis through inhibition reduction, providing a plausible first step toward potential, gradual endosymbiotic integration. Our work bridges the gap between models of microbial cooperation between free-living species and models that assume already-concluded, fully integrated endosymbiosis under multilevel selection. Author summary: Metabolic interactions among microbes are integral to their associations ranging from cross-feeding between free-living individuals to physically integrated cells. While metabolic coupling among free-living microbes is ubiquitous, the conditions that enable and facilitate a more intimate physical connection or even integration remain unclear. This is mostly because we do not know examples that demonstrate how the process unfolds and we lack intermediates of the most important and perhaps the first of such integrations: mitochondria. With the potential benefits of forming a higher unit of selection by prolonged association, we hypothesize that an evolutionary path could exist from free-living syntrophic partners toward obligate endosymbiosis through the intermediate stage of syntrophic ectosymbiosis. Here we provide a theoretical model that demonstrates that host-initiated ectosymbiosis can be stable, even when the cross-feeding with the bound symbionts is unilateral. Our results demonstrate that the physical association with a syntrophic partner is selected for as a mechanism to survive a self-produced toxic metabolite. Self-inhibition turns out to be crucial as the feeding symbiont reducing it effectively provides the necessary benefit for the host. Our model provides a potential mechanism of an ecological driver that could hypothetically lead to the endosymbiotic origin of mitochondria among prokaryotic partners (alphaproteobacterium and Asgard archaeon), without assuming a direct metabolic benefit for the host.
SN - 1553-7358
ER -