Exploring the onset of B₁₂‐based mutualisms using a recently evolved Chlamydomonas auxotroph and B₁₂‐producing bacteria

Abstract

Summary Cobalamin (vitamin B12) is a cofactor for essential metabolic reactions in multiple eukaryotic taxa, including major primary producers such as algae, and yet only prokaryotes can produce it. Many bacteria can colonize the algal phycosphere, forming stable communities that gain preferential access to photosynthate and in return provide compounds such as B12. Extended coexistence can then drive gene loss, leading to greater algal–bacterial interdependence. In this study, we investigate how a recently evolved B12‐dependent strain of Chlamydomonas reinhardtii, metE7, forms a mutualism with certain bacteria, including the rhizobium Mesorhizobium loti and even a strain of the gut bacterium E. coli engineered to produce cobalamin. Although metE7 was supported by B12 producers, its growth in co‐culture was slower than the B12‐independent wild‐type, suggesting that high bacterial B12 provision may be necessary to favour B12 auxotrophs and their evolution. Moreover, we found that an E. coli strain that releases more B12 makes a better mutualistic partner, and although this trait may be more costly in isolation, greater B12 release provided an advantage in co‐cultures. We hypothesize that, given the right conditions, bacteria that release more B12 may be selected for, particularly if they form close interactions with B12‐dependent algae.

Scarcity of fixed carbon transfer in a model microbial phototroph-heterotroph interaction

“…1C, p > 0.05). Although the maximum density of M. japonicum in coculture without sucrose (∼3x10 7 –5x10 8 CFU/ml) was similar to what has been observed previously [27], we found that the bacterium was able to achieve a comparable density without the alga.…”

“…5D). This demonstrated that greater algal density does not translate into greater M. japonicum growth, as noted previously [27].…”

A purine salvage bottleneck leads to bacterial adenine cross-feeding

“…Purine externalization is not dependent on E. coli or growth conditions. In some cross-feeding systems, the recipient can influence metabolite externalization by a producer (30)(31)(32). To test whether E. coli induces R. palustris purine externalization, we inoculated E. coli ΔpurH into media supplemented with R. palustris monoculture supernatant.…”

“…Genomic signatures could be more diverse than the repertoire of cross-fed metabolites. Metabolite externalization can also be conditional (2, 31, 32, 41) and need not even require a genetic signature in the producer. Previously we found that enhanced metabolite acquisition by a recipient was sufficient to stimulate more NH 4 + release by a producer and establish cross-feeding; the genetic signature was in the recipient (30).…”

Skin-associated Corynebacterium amycolatum shares cobamides

“…Yet, mass spectrometry revealed very low levels of cobalamin (a benzimidazolyl cobamide) in the same cell extracts, supporting this prediction. A wealth of studies exist that predict the existence of cobamide sharing between microorganisms (9,(11)(12)(13)(14)(15)(16)(17)42), and of these, a number provide direct experimental evidence for this phenomenon, although they are almost exclusively restricted to those between bacteria and cobamide-requiring eukaryotes (43)(44)(45)(46). Evidence of cobamide sharing between two or more bacterial species is limited, potentially due to a lack of experimental models to measure this phenomenon and the non-auxotrophic nature of many cobamide-utilizing bacteria (9).…”