Bacteriophage-mediated lysis supports robust growth of amino acid auxotrophs

Microbial communities host many auxotrophs-organisms unable to synthesize one or more metabolites required for their growth. Auxotrophy is thought to confer an evolutionary advantage, yet auxotrophs must rely on other organisms that produce the metabolites they require. The mechanisms of metabolite provisioning by producers remain unknown. In particular, it is unclear how metabolites such as amino acids and cofactors, which are found inside the cell, are released by producers to become available to auxotrophs. Here, we explore metabolite secretion and cell lysis as two distinct possible mechanisms that result in the release of intracellular metabolites from producer cells. We measured the extent to which secretion or lysis of Escherichia coli and Bacteroides thetaiotaomicron amino acid producers can support the growth of engineered Escherichia coli amino acid auxotrophs. We found that cell-free supernatants and mechanically lysed cells provide minimal levels of amino acids to auxotrophs. In contrast, bacteriophage lysates of the same producer bacteria can support as many as 47 auxotroph cells per lysed producer cell. Each phage lysate released distinct levels of different amino acids, suggesting that in a microbial community the collective lysis of many different hosts by multiple phages could contribute to the availability of an array of intracellular metabolites for use by auxotrophs. Based on these results, we speculate that viral lysis could be a dominant mechanism of provisioning of intracellular metabolites that shapes microbial community structure.

Automated summary

Microbial communities often contain auxotrophs, organisms that cannot synthesize certain metabolites necessary for growth. This study investigates the mechanisms by which these metabolites are released from producer cells to be utilized by auxotrophs. The researchers found that cell lysis by bacteriophages could be a dominant mechanism of metabolite provisioning in microbial communities. These findings suggest that the collective lysis of different hosts by multiple phages contributes to the availability of intracellular metabolites for auxotrophs.