Obligate cross-feeding expands the metabolic niche of bacteria

Abstract

Bacteria frequently engage in obligate metabolic mutualisms with other microorganisms. However, it remains generally unclear how the resulting metabolic dependencies affect the ecological niche space accessible to the whole consortium relative to the niche space available to its constituent individuals. Here we address this issue by systematically cultivating metabolically dependent strains of different bacterial species either individually or as pairwise coculture in a wide range of carbon sources. Our results show that obligate cross-feeding is significantly more likely to expand the metabolic niche space of interacting bacterial populations than to contract it. Moreover, niche expansion occurred predominantly between two specialist taxa and correlated positively with the phylogenetic distance between interaction partners. Together, our results demonstrate that obligate cross-feeding can significantly expand the ecological niche space of interacting bacterial genotypes, thus explaining the widespread occurrence of this type of ecological interaction in natural microbiomes.

Metabolic dissimilarity determines the establishment of cross-feeding interactions in bacteria

“…In contrast, two phylogenetically distant strains likely differ in their metabolic capabilities and requirements. Thus, two more closely related strains are likely to compete for environmentally available nutrients and provide an increased potential for a difference in the cost-to-benefit-ratio than two distant relatives [43, 61, 62]. This statistical relationship can explain why in our coculture experiments, both the phylogenetic and metabolic distance were positively associated with the growth of cocultured auxotrophs.…”

Microbial mutualism generates multistable and oscillatory growth dynamics

“…The community considered here provides a simplified representation of the aerobe-anaerobe communities that play critical roles in human health, our environment, waste treatment, and other biotechnological processes 2,4,5,7,11,[39][40][41][42][43][44][45][46][47][48][49][50][51][52][53][54][55][65][66][67][68][69][70][71][72][73][74][76][77][78][79][80][81][82][83][84][85][86][87][88] ; thus, our work sets a foundation for future research with potential implications extending beyond microbiology and biological physics. To this end, our model takes a step toward capturing the essential biophysical processes underlying the complex dynamics of such microbial communities-but in doing so, necessarily required some simplifying assumptions and approximations.…”

“…The bacteria are described by a number concentration b with subscripts aer and an for aerobes and anaerobes, respectively. Genome sequencing and metabolic profiling of such communities indicate that the consumption and secretion of only a small number of metabolites often drives experimental outcomes [3][4][5]7,13,94 -providing a clue that the full network of metabolic interactions could be dramatically simplified while still generating realistic community behaviors. Hence, inspired by 2 , we focus on the case in which the anaerobes take up an exogenously-supplied complex carbohydrate (teal) that cannot be accessed by the aerobes, breaking it down into simple sugar molecules (green) that they either directly consume for their growth or liberate to be consumed by the entire microbial community; for simplicity, we do not con-sider any other compounds, such as short-chain fatty acids, that may also liberated upon carbohydrate breakdown.…”

“…This network of interactions can give rise to fascinating emergent behaviors whose occurrence is remarkably consistent across diverse communities. For example, a common finding is that microbial communities can have multiple stable states, each characterized by its own unique composition of the different coexisting species, and each of which is stable under different environmental conditions [1][2][3][4][5][6][7][8][9][10][11][12][13][14][15] . In some cases, these states are multistable-i.e., multiple stable states can arise under identical conditions-leading, for example, to hysteretic behavior in which the state of the community depends not just on current conditions, but also on the history of how they were established [2][3][4]9,[16][17][18][19][20][21][22][23][24][25][26] .…”

Obligate mutualistic cooperation limits evolvability

“…weakest link hypothesis 15 ). Consequently, the niche space available to the whole association is reduced to an intersecting subset of the niche space accessible to the participating individuals 16, 17 . While some studies find indeed evidence that the survival of the whole interdependent consortium can be limited by the temperature tolerance of one of its partners 18, 19 , others report that mutualistic interactions can ameliorate environmental stress and thus even extent a species’ range limit 20 .…”