Prophages in Lactobacillus reuteri Are Associated with Fitness Trade-Offs but Can Increase Competitiveness in the Gut Ecosystem

Abstract

Bacteriophages derived from lysogens are abundant in gut microbiomes. Currently, mechanistic knowledge is lacking on the ecological ramifications of prophage carriage yet is essential to explain the abundance of lysogens in the gut. An extensive screen of the bacterial gut symbiont Lactobacillus reuteri revealed that biologically active prophages are widely distributed in this species. L. reuteri 6475 produces phages throughout the mouse intestinal tract, but phage production is associated with reduced fitness of the lysogen. However, phage production provides a competitive advantage in direct competition with a nonlysogenic strain of L. reuteri that is sensitive to these phages. This combination of increased competition with a fitness trade-off provides a potential explanation for the domination of lysogens in gut ecosystem and how lysogens can coexist with sensitive hosts.

New insights into intestinal phages

“…However, the presence of active prophages, which produce virions, has been demonstrated experimentally in almost all gut bacterial strain tested, suggesting that a significant proportion of prophages detected by genomic analyses are active. 33,34,37,38 High prevalence of temperate phages in human microbiota could participate in the stability of the phageome over time, as populations of lysogenic bacteria constantly produce virions. (4) The identity of the hosts targeted by the phages is a crucial but largely unanswered question.…”

“…Indeed, it has been shown in mouse models that a high prophage induction rate modifies the equilibrium between bacterial strains by disfavoring lysogens. 38,58 Lysogenic conversion Some prophages compensate their detrimental effects on their host by providing them beneficial traits that augment their fitness and can confer completely novel phenotypes, a phenomenon known as "lysogenic conversion." Examples of lysogenic conversion are numerous and recently reviewed by Taylor et al 69 and Wahl et al 70 in Salmonella.…”

Comparative Analysis of Lactobacillus gasseri and Lactobacillus crispatus Isolated From Human Urogenital and Gastrointestinal Tracts

“…It has been reported that prophages in Lactobacillus reuteri can be activated during GI transit, particularly in a fructose-enriched diet (Oh et al, 2019a). It was also reported that although prophages in L. reuteri 6475 were associated with a fitness trade-off, they can be advantageous in its intestinal niche by killing its competitors through generating active phages (Oh et al, 2019b). The different predicted prophage regions in the four Lactobacillus strains in our study likely reflect the different viral communities between human GI and vaginal tract.…”

The Diversity of the CRISPR-Cas System and Prophages Present in the Genome Reveals the Co-evolution of Bifidobacterium pseudocatenulatum and Phages

“…Meanwhile, bacterial hosts can acquire some novel functions and become more competitive in the community. For example, a prophage in Escherichia coli increases its host's resistance to antibiotics and oxidative stress (Wang et al, 2010); prophages within Enterococcus faecalis V583 encode platelet-binding-like proteins which were found to function in adhesion to human platelets (Matos et al, 2013); prophages in L. reuteri can be induced and released to kill competitor strains so as to be advantageous in intestinal niche (Oh et al, 2019b).…”