The peritoneal cestode Taenia crassiceps restructures gut bacterial communities in the mouse host: identification of potential resistance-associated bacteria

TL;DR

A peritoneal tapeworm alters gut bacteria in mice, with certain bacteria linked to resistance against the parasite.

Contribution

This study identifies potential resistance-associated bacteria modulated by a peritoneal cestode in mice.

Findings

NLRP3-deficient mice showed distinct gut microbiota with higher Akkermansia and Lachnospira.

Dubosiella abundance was inhibited by T. crassiceps infection but higher in resistant mice.

The peritoneal-gut axis modulates microbiota, influencing resistance and anti-inflammatory effects.

Abstract

Helminthic parasites cause chronic infections due to their ability to generate immune regulatory networks in their hosts; however, an additional component in this interplay is the microbiota. In this regard, new insights have emerged from intestinal helminthic infections, but whether extraintestinal worms are able to alter intestinal microbiota is unknown. Here, we explored microbiota changes occurring during experimental infection with the peritoneal, non-migrating cestode Taenia crassiceps. Our sequencing approach allowed for the identification of 56 families and 119 genera in the fecal samples. We compared the microbiota composition between wild-type (WT) and NLRP3-deficient mice (NLRP3−/−), since we recently reported that the lack of NLRP3 dramatically enhanced mouse resistance against T. crassiceps. Prior to T. crassiceps infection, NLRP3−/− mice harbored distinct microbial communities when compared to WT animals. The lack of NLRP3 resulted in enrichment of Akkermansia and Lachnospira, while reducing Clostridium, Dubosiella, and Bifidobacterium. Strikingly, Lactobacillus presented a comparable abundance in uninfected WT and NLRP3−/− mice. Upon infection, a progressive increase in Akkermansia and a transitory expansion of Lachnospiraceae were observed in WT mice but not in NLRP3−/− mice. A remarkable finding was that T. crassiceps infection inhibited Dubosiella, whereas the groups with enhanced resistance to T. crassiceps (NLRP3−/− mice and WT individuals co-housed with NLRP3−/− mice) presented a greater abundance of Dubosiella, indicating that resistance against T. crassiceps might be coordinated by this bacterium. Our study reveals that intestinal microbiota can also be modulated through a peritoneal-gut axis, in which the players (antigens and immune cells) remain to be identified. In addition to resistance, microbiota changes could be involved in the T. crassiceps-evoked anti-inflammatory and anti-oncogenic effects.

The online version contains supplementary material available at 10.1007/s00436-025-08574-1.

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