Evolution of bidirectional costly mutualism from byproduct consumption

Harcombe, William R.; Chacón, Jeremy M.; Adamowicz, Elizabeth M.; Chubiz, Lon M.; Marx, Christopher J.

doi:10.1073/pnas.1810949115

Cited by 103 publications

(115 citation statements)

References 25 publications

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“…Understanding the nature of the costs and benefits accrued to individuals involved in interspecific exchanges is crucial for explaining the diversity and stability of mutualisms in microbial communities (e.g. Harcombe 2010, Rakoff-Nahoum et al 2016, Harcombe et al 2018. In rate mutualisms, the return benefits materialise quicker than in yield mutualisms, and so rate mutualisms are favoured at early stages of community growth (i.e.…”

Section: Discussionmentioning

confidence: 99%

“…In the majority of these cases, the most parsimonious explanation is that the secreted factor serves to aid a conspecific (or even the focal producer cell), posing little dilemma if the anticipated recipient likely carries a copy of the gene coding for the trait. However, there are exceptions where the costly secreted factor provides benefits that are targeted to another strain or species (Harcombe 2010, Pande et al 2014, Rakoff-Nahoum et al 2016, Harcombe et al 2018.The interspecific exchange of costly secretions seems to be at odds with the Darwinian theory of adaptation by natural selection, which posits that selfishness should be rife in the natural world…”

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confidence: 99%

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Community lifespan, niche expansion and the evolution of interspecific cooperation

Rodrigues

Estrela

Brown

2020

Preprint

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Natural selection favours individuals who maximise their own reproductive success and that of their close relatives. From this perspective, cooperation that benefits individuals of a different species represents an evolutionary conundrum. The theory of mutualism seeks to resolve this puzzle, and it posits that there must be downstream benefits to cooperators that offset any costs inherently associated with interspecific cooperation. Thus, individuals should only further the survival and fecundity of their interspecific partners if this generates additional return benefits, such as food, shelter or protection. A major challenge for the evolution of mutualism is when the ecological niches of partner species overlap, as this creates a tension between the benefits of exchanging services and the costs of competing for shared resources. Here we study the extent to which niche expansion, in which cooperation augments the common pool of resources, can resolve this problem. We find that niche expansion facilitates the evolution of mutualism, especially when populations are at high densities. Further, we show that niche expansion can promote the evolution of reproductive restraint, in which a focal species adaptively sacrifices its own growth rate to increase the density of partner species. We interpret these results in the context of microbial community interactions, which are often characterized by yieldenhancing exchanges of nutrients, termed 'cross-feeding'. Our findings suggest that yieldenhancing mutualisms are more prevalent in stable habitats with a constant supply of resources, where populations typically live at high densities, but such mutualisms are particularly vulnerable to the emergence of cheats. In general, our findings highlight the need to integrate both temporal and spatial dynamics in the analysis of mutualisms.Keywords -demography, ecology, mutualism, cross-feeding, kin selection, spatial structure. al. 2016) and among partner species engineered (Shou et al. 2007, Wintermute and Silver 2010, Mee et al. 2014) and evolved in the lab (Harcombe 2010, Pande et al. 2014, Harcombe et al. 2018). These examples pose the question of whether costly microbial mutualisms are more widespread and awaiting discovery. To approach this question, we ask what ecological conditionsare most likely to support these mutualistic investments?Microbial cells release compounds into their environment that are then used by other members of the community for survival and growth Brown 2015, Estrela et al. 2019). In some cases (termed cross-feeding or syntrophy), these exo-molecules are a waste product of an individual's metabolism that is advantageously co-opted by a partner species (Hillesland and Stahl 2010, Estrela et al. 2012, LaSarre et al. 2017, Goldford et al. 2018, and as such, it comes at no cost to the producer. More challenging for evolutionary theory is when the exchanged compounds are not simple metabolic waste products but specifically designed costly secretions, such as the secretion of nutrient-scavenging molecules ...

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

Community lifespan, niche expansion and the evolution of interspecific cooperation

Rodrigues

Estrela

Brown

2020

Preprint

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“…[ 28 ] Rapid evolution of prokaryotic trade, starting with the use of the waste product of one participant, but ending with populations in which both partners secrete costly products, has even been observed in laboratory settings. [ 29–31 ] An important precondition for these stable symbioses to take hold is that they occur in spatially structured environments. There are different scenarios for the primordial symbiosis giving rise to eukaryogenesis, such as the “hydrogen hypothesis” [ 24 ] (named after the waste product involved) or alternating cellular electron‐acceptors operating in the presence of varying amounts of oxygen (with intermediate metabolites as waste).…”

Section: Predator or Parasite Models Of Eukaryogenesis Have Conceptuamentioning

confidence: 99%

“…Harcombe, Marx, and co‐workers have been performing experiments to define parameters conductive to symbiosis, using different bacterial strains. [ 29,31 ] What would happen during the co‐culture of non‐O 2 using archaea and oxidizing bacteria under fluctuating O 2 ? In other model systems, what will happen to membrane potentials and ROS formation in mitochondria missing UCP “safety valves”?…”

Section: Is This Indeed How Eukaryotes Evolved (Future Experiments Anmentioning

confidence: 99%

Debating Eukaryogenesis—Part 1: Does Eukaryogenesis Presuppose Symbiosis Before Uptake?

Speijer

2020

BioEssays

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Eukaryotic origins are heavily debated. The author as well as others have proposed that they are inextricably linked with the arrival of a pre‐mitochondrion of alphaproteobacterial‐like ancestry, in a so‐called symbiogenic scenario. The ensuing mutual adaptation of archaeal host and endosymbiont seems to have been a defining influence during the processes leading to the last eukaryotic common ancestor. An unresolved question in this scenario deals with the means by which the bacterium ends up inside. Older hypotheses revolve around the application of known antagonistic interactions, the bacterium being prey or parasite. Here, in reviewing the field, the author argues that such models share flaws, hence making them less likely, and that a “pre‐symbiotic stage” would have eased ongoing metabolic integration. Based on this the author will speculate about the nature of the (endo) symbiosis that started eukaryotic evolution–in the context of bacterial entry being a relatively “early” event–and stress the differences between this uptake and subsequent ones. He will also briefly discuss how the mutual adaptation following the merger progressed and how many eukaryotic hallmarks can be understood in light of coadaptation. Also see the video abstract here https://youtu.be/ekqtNleVJpU

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“…While this method has been used mainly to look at the evolution 160 of single species, an increasing number of studies employs simple two-species communities 161 to ask how species evolve in the presence of a coevolutionary partner [49]. Mostly, these 162 experiments focus on the evolution of species with a predefined interspecific relationship-163 such as host-parasite [50], predator-prey [51], or mutualism [52,53]-and assess how 164 interaction traits like parasite infectivity and host defence change over evolutionary time. At 165 least two studies explicitly report a change in the nature of the interactions between two 166 species: in one case, a commensal interaction quickly evolved into exploitation [54], whereas 167 in the other case, ammensalism evolved into antagonism [55].…”

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Understanding the evolution of interspecies interactions in microbial communities

Gorter

Manhart

Ackermann

2019

Preprint

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20Microbial communities are complex multi-species assemblages that are characterized by a 21 multitude of interspecies interactions, which can range from mutualism to competition. The 22The next step will be to test these hypotheses experimentally and provide input for a more 38 refined version of the model in turn, thus closing the scientific cycle of models and 39 experiments. 40 control the processes that they mediate [7,8]. 51 52 Microbial communities, like all complex systems, are more than the sum of their parts: they 53 are characterized by a multitude of often complex interactions between their constituent 54 members (Figure 1). At any given time, microbes may compete for shared resources such as 55 metabolites and space, inhibit each other via the secretion of antibiotics and other toxic 56 compounds, and even kill each other upon direct cell-cell contact[9,10]. Yet, not all is bleak 57in the microbial world: some organisms may-accidentally or actively-excrete enzymes or 58 molecules that others can use, and even commit suicide for others [11][12][13]. The overall sign 59 and strength of an interaction between two organisms is the net result of all such processes 60 and can be characterised as anything from competition to parasitism and mutualism [14,15]. 61 62Interspecific interactions have a crucial role to play in microbial communities. That is, what 63 makes a community a community-rather than a random set of species-is precisely these 64 interactions, because they give rise to properties at the level of the community that we cannot 65 understand by considering each species in isolation. For example, it may not be possible to 66 predict from growing each species by itself what the joint reproductive output of a collective 67 will be, or how robust such a collective will be to external biotic and abiotic perturbations. 68Microbial communities can also perform chemical transformations that would be impossible 69 for one individual species to achieve[16], and some communities even display complex 70 behaviours such as collective motion and electrochemical signalling, which have traditionally 71 been associated with higher organisms [17,18]. 72 73Over the past decades, an impressive amount of thought and effort has been dedicated 74 towards obtaining an ever-more detailed and realistic picture of a wide range of different 75

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Evolution of bidirectional costly mutualism from byproduct consumption

Cited by 103 publications

References 25 publications

Community lifespan, niche expansion and the evolution of interspecific cooperation

Community lifespan, niche expansion and the evolution of interspecific cooperation

Debating Eukaryogenesis—Part 1: Does Eukaryogenesis Presuppose Symbiosis Before Uptake?

Understanding the evolution of interspecies interactions in microbial communities

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