Understanding the Mechanisms of Positive Microbial Interactions That Benefit Lactic Acid Bacteria Co-cultures

Abstract

Microorganisms grow in concert, both in natural communities and in artificial or synthetic co-cultures. Positive interactions between associated microbes are paramount to achieve improved substrate conversion and process performance in biotransformation and fermented food production. The mechanisms underlying such positive interactions have been the focus of numerous studies in recent decades and are now starting to be well characterized. Lactic acid bacteria (LAB) contribute to the final organoleptic, nutritional, and health properties of fermented food products. However, interactions in LAB co-cultures have been little studied, apart from the well-characterized LAB co-culture used for yogurt manufacture. LAB are, however, multifunctional microorganisms that display considerable potential to create positive interactions between them. This review describes why LAB co-cultures are of such interest, particularly in foods, and how their extensive nutritional requirements can be used to favor positive interactions. In that respect, our review highlights the benefits of co-cultures in different areas of application, details the mechanisms underlying positive interactions and aims to show how mechanisms based on nutritional interactions can be exploited to create efficient LAB co-cultures.

Keywords: co-culture; cross-feeding; lactic acid bacteria; metabolic dependencies; microbial community; positive interactions; public goods.

FIGURE 1

Types of microbial communities and co-cultures, their use, benefits and some examples of their areas of application. Natural community: a self-assembled association of environmental microbes found in various ecosystems. Enriched natural community: a selection of specific microbes belonging to a natural community. Artificial co-culture: an association of microorganisms that may not necessarily be found in nature. Synthetic co-culture: an association of microorganisms in which at least one of the strains is a genetically modified organism.

FIGURE 2

Schematic representation of the four types of interactions resulting in positive outcomes for the microorganisms involved. ➀ Commensalism: increased fitness of one interacting partner without affecting the second. ➁ Cooperation: the two interacting partners share the same phenotype and improve each other’s fitness. ➂ Mutualism: the increased fitness of two interacting partners that do not benefit from the same molecules. ➃ Syntrophy: one cell benefits from the metabolites produced by the other, and meanwhile removes the inhibition induced by these metabolites for the producer. The dotted lines between mutualism and syntrophy, and mutualism and cooperation, mean that they are both particular forms of mutualism. Interactions ➁ to ➃ are bidirectional.

FIGURE 3

Decision tree to characterize the mechanism underlying positive interactions between two microorganisms. The dotted squares contain preliminary questions to establish whether this is a case of positive interaction or not, or supplementary questions to establish its type. In the case of bidirectional interactions, the decision tree can be read twice: the first reading aims to characterize the effect of microorganism A on B (plain arrows), and the second aims to characterize the effect of B on A (dotted arrows). The sequential questions are designed to establish whether the interaction:

1. –

   is direct or indirect,

2. –

   engages a sharing of public goods or is due to physicochemical changes in the medium,

3. –

   is reliant on secreted primary metabolites or not.