Understanding the evolution of interspecies interactions in microbial communities

Abstract

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

Ecology and evolution of antimicrobial resistance in bacterial communities

“…In contrast, if protection is provided by multiple species present in the community, or by the physical properties of the community (e.g., biofilm matrix), collective resistance or tolerance would likely be more stable due to relatively higher functional redundancy of “protection” within the community. Ecological stability of collective resistance and collective tolerance could thus alter the length of antibiotic exposure, and therefore alter the timescales in which selection for resistance can act [ 67 , 68 ]. Inactivation of antibiotics may result in transient and short-lived antibiotic exposure leading to changes at ecological rather than evolutionary timescales, that is, changes in the composition and frequencies of different species within the community similar to the effect of ecological disturbances.…”

Physical connections: prokaryotes parasitizing their kin

“…Together with abiotic factors, species interactions determine community structure (Little et al ., 2008; Nadell et al ., 2016) and impact evolution (Celiker and Gore, 2013; Mitri and Foster, 2013). The positive or negative influence and the strength of direct and indirect interactions in communities may vary with space and time, although how time regulates interactions is not yet well understood (Gorter et al ., 2020). Ultimately, the selection of traits and, hence, the nature of interactions depend on the environment, which may favour or disfavour relations depending on their effects on fitness (Fig.…”

Higher-order effects, continuous species interactions, and trait evolution shape microbial spatial dynamics

“…Prior studies of community-level eco-evolutionary dynamics, which have explored the evolution of species interactions abstractly or the specific traits that determine such interactions (43–45), focused on niche-based food web models (i.e., those involving resource consumption) rather than the non-resource based antagonistic interactions that characterize our work. Even when studies did investigate antagonistic interactions and resultant species dynamics, they emphasized very slow mutation regimes and assumed a separation of ecological and evolutionary timescales (46–48). Such assumptions do not work very well for microbial systems, where high mutation rates and extensive horizontal gene transfers are commonplace, creating an overlap of ecological and evolutionary timescales (47–50).…”

“…Such assumptions do not work very well for microbial systems, where high mutation rates and extensive horizontal gene transfers are commonplace, creating an overlap of ecological and evolutionary timescales (47–50). These eco-evolutionary feedbacks can affect the nature of trait evolution (48) and even destabilize species interactions (51). Recent models exploring these fast-evolving regimes in antibiotic-mediated antagonistic communities have uncovered mechanisms responsible for de novo assembly of diverse microbial communities with higher-order interactions, but such results are qualitatively different from what is possible when mutation is rare (38, 47).…”