Food-spoilage-associated Leuconostoc, Lactococcus, and Lactobacillus species display different survival strategies in response to competition.

Psychrotrophic lactic acid bacteria (LAB) are the prevailing spoilage organisms in packaged cold-stored meat products. Species composition and metabolic activities of such LAB spoilage communities are determined by the nature of meat product, storage condition and interspecies interactions. Our knowledge of systems-level responses of LAB during such interactions is very limited. To expand it, we studied interactions between three common psychrotrophic spoilage LAB ( Leuconostoc gelidum , Lactococcus piscium and Lactobacillus oligofermentans ) by comparing their time-course transcriptome profiles obtained during their growth in individual, pairwise and triple cultures. The study revealed how these LAB employed different strategies to cope with the consequences of interspecies competition. The fastest growing bacterium, Le. gelidum, attempted to enhance its nutrient-scavenging and growth capabilities in the presence of other LAB through upregulation of the carbohydrate catabolic pathways, pyruvate fermentation enzymes and ribosomal proteins. Whereas, the slower growing Lc. piscium and Lb. oligofermentans downregulated these functions. These findings may explain the competitive success and predominance of Le. gelidum in a variety of spoiled foods. Peculiarly, interspecies interactions induced overexpression of prophage genes and restriction-modification systems (mechanisms of DNA exchange and protection against it) in Lc. piscium and Lb. oligofermentans, but not in Le. gelidum . Co-cultivation induced also overexpression of the numerous putative adhesins in Lb. oligofermentans. These adhesins might contribute to the survival of this slowly growing bacterium in actively growing meat spoilage communities. Importance Despite the apparent relevance of LAB for biotechnology and human health, interactions between members of LAB communities are not well known. Knowledge of such interactions is crucial for understanding how these communities function and, consequently, whether there is any possibility to develop new strategies to interfere with the growth and to postpone spoilage of packaged and refrigerated foods. With the help of controlled experiments detailed regulation events can be observed. This study gives an insight into the system-level interactions and the different competition-induced survival strategies related to enhanced uptake and catabolism of carbon sources, overexpression of adhesins and putative bacteriocins, and to the induction of exchange of genetic material. Even though this experiment dealt only with three LAB strains in vitro , these findings agreed well with the relative abundance patterns typically reported for these species in natural food microbial communities.