Ecology and evolution of metabolic cross-feeding interactions in bacteria

Abstract

Literature covered: early 2000s to late 2017Bacteria frequently exchange metabolites with other micro- and macro-organisms. In these often obligate cross-feeding interactions, primary metabolites such as vitamins, amino acids, nucleotides, or growth factors are exchanged. The widespread distribution of this type of metabolic interactions, however, is at odds with evolutionary theory: why should an organism invest costly resources to benefit other individuals rather than using these metabolites to maximize its own fitness? Recent empirical work has shown that bacterial genotypes can significantly benefit from trading metabolites with other bacteria relative to cells not engaging in such interactions. Here, we will provide a comprehensive overview over the ecological factors and evolutionary mechanisms that have been identified to explain the evolution and maintenance of metabolic mutualisms among microorganisms. Furthermore, we will highlight general principles that underlie the adaptive evolution of interconnected microbial metabolic networks as well as the evolutionary consequences that result for cells living in such communities.

Nanotube‐mediated cross‐feeding couples the metabolism of interacting bacterial cells

“…Bacteria often engage in metabolic cross-feeding interactions with other bacteria and eukaryotic organisms (Kiers et al, 2003;Belenguer et al, 2006;Vogel and Moran, 2011;Johnson et al, 2012;McFall-Ngai, 2014;Seth and Taga, 2014;Ponomarova and Patil, 2015;Zelezniak et al, 2015;Estrela et al, 2016;D'Souza et al, 2018). In many of these cases, two or more interacting partners reciprocally exchange primary building block metabolites such as amino acids (Payne et al, 1957;Junglas et al, 2008;Sieuwerts et al, 2010;Vogel and Moran, 2011;Garcia et al, 2015), vitamins (Croft et al, 2005;Rodionova et al, 2015), or even nucleotides (Sieuwerts et al, 2010;Dean et al, 2016;Loera-Muro et al, 2016).…”

Metabolic exchange and energetic coupling between nutritionally stressed bacterial species, the possible role of QS molecules

“…In some cases, the interactions between C. acetobutylicum and D. vulgaris, resembled those described by Dubey and Ben-Yehuda 10 . Moreover, this type of cellcell interactions has been seen also in other systems, which give support to its existence and functionality 10,13 .…”

“…In some cases, the interactions between C. acetobutylicum and D. vulgaris, resembled those described by Dubey and Ben-Yehuda 10 . Moreover, this type of cellcell interactions has been seen also in other systems, which give support to its existence and functionality 10,13 .Nutritional stress appears crucial to induce physical contact between bacteria, as this interaction was prevented by the presence of lactate and sulfate, nutrients of D. vulgaris.Furthermore, Pande et al 20 in a synthetic co-culture of E. coli and Acinetobacter baylyi, after depletion of aminoacids such as histidine and tryptophan by genetic manipulation, observed nanotubular structures between the auxotrophs allowing cytoplasmic exchange. As in our case, the communication between the mutants was prevented by the presence of the nutrients.The formation of nanotubes between aminoacid-starved bacteria might be a strategy to survive under aminoacid limiting conditions 13 .…”

“…Dubey and Ben-Yehuda 10 were the first to demonstrate a contact-dependent exchange of cytoplasmic molecules via nanotubes in Bacillus subtilis which contributes to proper colony formation 11,12 . The evolution of how metabolites came to be transferred between bacteria, and its functioning today, were both well described in a recent review 13 .…”

Cooperation of partially-transformed clones: an invisible force behind the early stages of carcinogenesis

“…While the mathematical analysis we presented was not elaborated to capture more complex phenomena occurring during oncogenesis, our model highlights the importance of identifying the genes and the shared resources that can mediate clonal cooperation, such as growth factors (e.g., mitogens, interleukins, etc.) or even metabolic by-products that are often at the basis of cooperative behaviour in lower organisms [37][38][39] . The theory described here was aimed to be simple and, at the best of our knowledge, it is a first attempt to describe the problem with an explicit mathematical model to extend the existing models of oncogenesis 11,22,[40][41][42][43] to nonautonomous mechanisms.…”