Exploitation by cheaters facilitates the preservation of essential public goods in microbial communities

Abstract

29How are public goods 1-4 maintained in bacterial cooperative populations? The presence of 30 these compounds is usually threatened by the rise of cheaters that do not contribute but 31 just exploit the common resource 5,6 . Minimizing cheater invasions appears then as a 32 necessary maintenance mechanism 7,8 . However, that invasions can instead add to the 33 persistence of cooperation is a prospect that has yet remained largely unexplored 6 . Here, 34we show that the detrimental consequences of cheaters can actually preserve public goods, 35at the cost of recurrent collapses and revivals of the population. The result is made 36 possible by the interplay between spatial constraints and the essentiality of the shared 37 resource. We validate this counter-intuitive effect by carefully combining theory and 38 experiment, with the engineering of an explicit synthetic community in which the public 39compound allows survival to a bactericidal stress. Notably, the characterization of the 40 experimental system identifies additional factors that can matter, like the impact of the lag 41 phase on the tolerance to stress, or the appearance of spontaneous mutants. Our work 42 emphasizes the unanticipated consequences of the eco-evolutionary feedbacks that emerge 43 in microbial communities relying on essential public goods to function, feedbacks that 44 reveal fundamental for the adaptive change of ecosystems at all scales. 45 46 47 48 49 50 51 52 53 54 55 3 Main text 56 57The threat of cheaters represents at a microbial scale a well-known public good 58 (PG) dilemma, known as the "tragedy of the commons" 9 , and can fundamentally interfere 59 with the sustainability of microbial communities. The necessity of recognizing the 60 consequences of social dilemmas in microorganisms thus becomes essential, given their 61 impact in many aspects of life on Earth, and also its particular relevance to humans in 62 matters of health (microbiome) 10 , and industry (bioremediation, biofuels, etc) 11 . We 63 considered specifically a scenario in which a community is organized as a dynamical 64 metapopulation (i.e., the community is transiently separated into groups) 12 , and the action 65 of a PG is essential for its survival. Spatial structure is a well-known universal mechanism 66to promote cooperation 13 , which frequently emerges in bacterial populations, for instance, 67due to the restricted range of microbial interactions 14,15 . However, it is much less 68 understood how the presence of structure affects the maintenance of cooperation when 69 combined with explicit population dynamics (earlier work usually assumed constant 70 population and only examined evolutionary dynamics) 16 . The change in population size 71associated to the essentiality of the PG can indeed bring about complex eco-evolutionary 72 feedbacks 17-20 , in which both population density and frequency of "cooperators" influence 73 each other. The connection between these feedbacks and spatial structure remains thus an 74open problem that has started to be addres...

Antibiotic Stress Selects against Cooperation in a Pathogenic Bacterium

“…This raises the question of how the two types can coexist (resulting in more virulent infections) as has been observed in situ (56). A reasonable hypothesis is spatial structure (57)(58)(59)(60), whereby spatial segregation of non-producers and producers limits the exploitative potential of the former. Future theoretical and experimental study is needed to test this prediction.…”

Antibiotic stress selects against cooperation in the pathogenic bacterium Pseudomonas aeruginosa

“…13). In many cases, a likely important factor enabling coexistence is spatial structure (62)(63)(64), whereby spatial segregation of nonproducers and producers limits the exploitative potential of the former. In one of the few studies investigating interactions between antibiotics and social behaviors in bacteria, Diard et al (14) assessed the in vivo impact of ciprofloxacin on competition between virulent cooperative Salmonella enterica serovar Typhimurium and avirulent defectors.…”

Limited Pairwise Synergistic and Antagonistic Interactions Impart Stability to Microbial Communities

“…These assemblies comprise of large number of genomes and are engaged in a number of antagonistic and synergistic interactions between participating species (Faust and Raes, 2012;Corel et al, 2016). Via these interactions, the participating species can change the physical, chemical, and biological environment, and thus, influence the growth of all members of the environment (Andrade-Dominguez et al, 2014;Moreno-Fenoll et al, 2017). The altered environment can, in turn, also impacts the strength of interactions between species (Ratzke et al, 2020).…”