Lactobacilli and other gastrointestinal microbiota of Peromyscus leucopus, reservoir host for agents of Lyme disease and other zoonoses in North America

Abstract

The cricetine rodent Peromyscus leucopus is an important reservoir for several human zoonoses, including Lyme disease, in North America. Akin to hamsters, the white-footed deermouse has been unevenly characterized in comparison to the murid Mus musculus. To further understanding of P. leucopus' total genomic content, we investigated gut microbiomes of an outbred colony of P. leucopus, inbred M. musculus, and a natural population of P. leucopus. Metagenome and whole genome sequencing were combined with microbiology and microscopy approaches. A focus was the genus Lactobacillus, four diverse species of which were isolated from forestomach and feces of colony P. leucopus. Three of the species-L. animalis, L. reuteri, and provisionally-named species "L. peromysci"-were identified in fecal metagenomes of wild P. leucopus but not discernibly in samples from M. musculus. L. johnsonii, the fourth species, was common in M. musculus but absent or sparse in wild P. leucopus. Also identified in both colony and natural populations were a Helicobacter sp. in feces but not stomach, and a Tritrichomonas sp. protozoan in cecum or feces. The gut metagenomes of colony P. leucopus were similar to those of colony M. musculus at the family or higher level and for major subsystems. But there were multiple differences between species and sexes within each species in their gut metagenomes at orthologous gene level. These findings provide a foundation for hypothesis-testing of functions of individual microbial species and for interventions, such as bait vaccines based on an autochthonous bacterium and targeting P. leucopus for transmission-blocking.

An Infection-Tolerant Mammalian Reservoir for Several Zoonotic Agents Broadly Counters the Inflammatory Effects of Endotoxin

“…Figure 1B summarizes the experimental design, and Table A1 in the appendix lists the characteristics of the animals in the experiment and selected parameters. Fecal samples obtained from animals a day before the experiment had been subjected to gut microbiome analysis (35), and alpha-diversity values of the microbiota from the earlier study are provided in the table. The animals of each species were sexually mature adults and comparable in size and age, though P. leucopus tended to be smaller and older by 1 to 2 weeks.…”

“…Could observed differences between the two species in these experiments be attributable in part to differences in their microbiomes? The gut metagenomes were determined from preexperiment fecal pellets from the animals in this study (35). In general, the deermice and mice had similar distributions and frequencies of bacteria at the taxonomic level of the family and in the representation and proportions of different biosynthetic, metabolic, catabolic, and regulatory functions, but there were also substantive differences in the gut microbiotas between the species that plausibly account for some distinguishing responses to LPS.…”

The infection-tolerant mammalian reservoir of Lyme disease and other zoonoses broadly counters the inflammatory effects of endotoxin

“…Could observed differences between the two species in these experiments be attributable in part to differences in their microbiomes? The gut metagenomes were determined from preexperiment fecal pellets from the animals in this study, and the results have been reported [38]. In general, the deermice and mice had similar distributions and frequencies of bacteria at the taxonomic level of family and in the representation and proportions of different biosynthetic, metabolic, catabolic, and regulatory functions.…”

“…The presence of Tritrichomonas muris in some populations of the same inbred strains of M. musculus altered their cellular immune responses to other microorganisms and antigens [93]. Further distinguishing the gut microbiota was the greater abundance and diversity in P. leucopus of Lactobacillus spp., the primary niche for which was the forestomach [38]. In two studies of the use of Lactobacillus spp.…”

“…Tables S1 and S21 of Supplementary Materials respectively provide information on each of the animals in the LPS experiments and corresponding National Center for Biotechnology Information (NCBI) (http://ncbi.nlm.nih.gov) BioProject and BioSample identifying numbers and descriptions for these samples. The gut metagenomes from feces collected from the 20 P. leucopus and 20 M. musculus animals 1-2 days before the comparative experiment have been described [38] and are available from MG-RAST database (https://www.mg-rast.org) under accession numbers mgm4832531.3-mgm4832578.…”