Abstract
Lactic acid bacteria (LAB) differ in their ability to colonize food and animal-associated habitats: while some species are specialized and colonize a limited number of habitats, other are generalist and are able to colonize multiple animal-linked habitats. In the current study, Carnobacterium was used as a model genus to elucidate the genetic basis of these colonization differences. Analyses of 16S rRNA gene meta-barcoding data showed that C. maltaromaticum followed by C. divergens are the most prevalent species in foods derived from animals (meat, fish, dairy products), and in the gut. According to phylogenetic analyses, these two animal-adapted species belong to one of two deeply branched lineages. The second lineage contains species isolated from habitats where contact with animal is rare. Genome analyses revealed that members of the animal-adapted lineage harbor a larger secretome than members of the other lineage. The predicted cell-surface proteome is highly diversified in C. maltaromaticum and C. divergens with genes involved in adaptation to the animal milieu such as those encoding biopolymer hydrolytic enzymes, a heme uptake system, and biopolymer-binding adhesins. These species also exhibit genes for gut adaptation and respiration. In contrast, Carnobacterium species belonging to the second lineage encode a poorly diversified cell-surface proteome, lack genes for gut adaptation and are unable to respire. These results shed light on the important genomics traits required for adaptation to animal-linked habitats in generalist Carnobacterium.
Highlights
Lactic acid bacteria (LAB) include various genera and many species that have been investigated for decades because of their major role in food fermentations and their health benefit potential as probiotics
Metagenomic data for genes encoding 16S rDNA from 681 samples were analyzed with a focus on the genus Carnobacterium
The most abundant species was C. maltaromaticum accounting for 28–60% of Carnobacterium reads, followed by C. divergens (15–49%) and Carnobacterium spp. from lineages that have not yet been cultured and characterized (14–47% of Carnobacterium reads, depending on the sample origin)
Summary
Lactic acid bacteria (LAB) include various genera and many species that have been investigated for decades because of their major role in food fermentations and their health benefit potential as probiotics. To compensate the loss of these functions, genes encoding transporters for amino acids or carbohydrates were gained to allow growth in nutritional rich fermentation environments (Lorca et al, 2007) These genomic changes were accompanied by a specialization to food matrices, exemplified in dairy strains. Lactobacillus iners is described to solely colonize the vaginal cavity and harbors one of the smallest LAB genomes presumably because its niche specialization allowed a substantial genome reduction (Macklaim et al, 2011; Mendes-Soares et al, 2014) Another example is the GI tract symbiont Lactobacillus reuteri, which is characterized by different lineages each one being apparently adapted to one particular vertebrate host: rodent or human (Frese et al, 2011). The genomic traits responsible for adaptation to multiple animal-associated habitats are not clearly defined
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