Dysbiosis of fecal microbiota in cats with naturally occurring and experimentally induced Tritrichomonas foetus infection

Abstract

The protozoal pathogen Tritrichomonas foetus infects the colon of domestic cats and is a major cause of chronic colitis and diarrhea. Treatment failure is common, but antibiotics may improve clinical signs in a subset of cats, leading researchers to question involvement of the colonic microbiota in disease pathogenesis. Studies performed in women with venereal Trichomonas vaginalis infections have revealed that dysbiosis of host microbiota contributes to pathogenicity with similar findings also found in mice with intestinal Tritrichomonas musculis The aim of this study was to characterize differences in the fecal microbiota of cats with and without naturally occurring T. foetus infection and in a group of kittens prior to and after experimentally induced infection. Archived fecal DNA from cats undergoing testing for T. foetus infection (n = 89) and experimentally infected kittens (n = 4; at pre-, 2 weeks, and 9 weeks post-infection) were analyzed by sequencing of 16S rRNA genes. Amongst the naturally infected population, the genera Megamonas and Helicobacter were significantly increased in prevalence and abundance in cats testing positive for T. foetus infection. In the group of four experimentally infected kittens, fecal samples post-infection had significantly lower abundance of genus Dialister and Megamonas and greater abundance of the class Betaproteobacteria and family Succinivibrionaceae. We hypothesize that T. foetus promotes dysbiosis by competition for fermentable substrates used by these bacteria and that metabolic byproducts may contribute to the pathogenesis of colonic inflammation and diarrhea. Future studies are warranted for the measurement of fecal concentrations of microbial and protozoal metabolites in cats with T. foetus infection for the identification of potential therapeutic targets.

The commensal protistTritrichomonas musculusexhibits a dynamic life cycle that induces extensive remodeling of the gut microbiota

“…Here, we profiled the activities of T. mu during a new colonization event, and report its ability to reshape both resident bacterial composition and gene expression in healthy hosts, and more rapidly in those with a compromised immunemediated ability to regulate the microbiota. Protist-induced shifts in bacterial composition have previously been documented for other protozoa, including G. duodenalis, T. foetus and T. gondii, as well as in a recent study of T. mu 8,17,18,59 . Some of the compositional changes that we noted also occurred in the study by Wei et al, including a reduction of Lactobacillaceae and increase in Bacteroidetes and Parabacteroides abundances 17 .…”

Revisiting fecal metatranscriptomics analyses of macaques with idiopathic chronic diarrhoea with a focus on trichomonad parasites

“…In summary, these metatranscriptomics analyses of Trichomonads in the macaque gut have provided the first in vivo insight into Trichomonad mucosal colonization, which validates numerous in vitro studies (Müller, 1990 ; Kulda, 1999 ; Westrop et al ., 2017 ; Handrich et al ., 2019 ). Our findings support previous reports of Trichomonad–microbiota interactions (Ji et al ., 2020 ; Wei et al ., 2020 ; Bierlein et al ., 2021 ), and demonstrate that such interactions vary between parasite species and are highly context-dependent. Longitudinal studies, or those involving experimental Trichomonad infection, could be used to investigate causality and underlying mechanisms in the parasite–microbiota–disease interrelationship.…”

“…For example, T. vaginalis infection can induce dysbiotic changes in the urogenital tract (UGT) microbiota (Fichorova et al ., 2013 ). Such results have been validated in vivo in several Trichomonad species and hosts (Wei et al ., 2020 ; Bierlein et al ., 2021 ). Notably, Trichomonas gallinae infection was correlated with changes in the microbiota at local and distant mucosal sites in pigeon squabs (Ji et al ., 2020 ).…”

Randomized placebo-controlled trial of feline-origin Enterococcus hirae probiotic effects on preventative health and fecal microbiota composition of fostered shelter kittens

“…Based on 16S rRNA gene amplicon sequencing, administration of the E. hirae probiotic did not alter the predominant bacterial phyla present in feces which were similar to prior descriptions of the fecal microbiota in cats. These phyla were represented mainly by Firmicutes, Bacteroidetes, Proteobacteria, Actinobacteria , and Fusobacteria ( 20 , 52 – 56 ). The presence of E. hirae also did not affect the overall number or diversity of different taxa present in the microbial community which is a desirable attribute of a probiotic.…”

“…In prior reports, dietary supplementation with fermentable prebiotics increased the abundance of Megamonas ( 57 – 59 ) while decreased in abundance of Megamonas have been described in cats with diarrhea ( 60 ). Interestingly, Megamonas was increased in feces of cats that were naturally infected with the diarrheal pathogen Tritrichomonas foetus , but decreased in feces of cats experimentally infected with the same pathogen ( 56 ). These collective observations suggest a vulnerability of Megamonas to specific, albeit unidentified changes in the feline intestinal tract.…”