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Parasites and diet as main drivers of the Malagasy gut microbiome richness and function.

ABSTRACT: Interactions between the prokaryotic microbiome and eukaryotic parasites in the vertebrate gut may affect overall host health and disease. While intertropical areas exhibit a high rate of parasites carriers, such interactions are understudied in these populations. Our objectives were to (1) describe the gut microbiome of individuals living in Madagascar, (2) identify potential associations between bacterial taxa and parasites colonizing the digestive tract and (3) highlight main determinants of the gut microbiota composition in this developing country. Metadata (socioeconomic, diet, clinical) and fecal samples were collected from 219 volunteers from North-West Madagascar (Mahajanga). Fecal microbiome was assessed through 16S rRNA gene sequencing and metabolomics, and related to dietary habits and parasites carriage. We highlight important Malagasy gut microbiome peculiarities. Out of three detected enterotypes, only one is similar to that observed in Westernized countries (Ruminococcus-driven). Functions associated with the two others (Clostridium sensu stricto-driven and Escherichia/Shigella-driven) are mostly directed toward amino acids biosynthesis and degradation, respectively. Diet and protozoan carriage were the main drivers of microbiota composition. High protozoan carriage was associated with higher diversity, richness and microbial functionalities. The gut microbiome of Malagasy strongly differs from that of Westernized countries. Asymptomatic protozoan carriage and dietary habits are the external factors with the deepest impact on gut microbiome. Further studies are needed to understand whether gut microbial richness constitute a predilection niche for protozoans colonization, due to their gazing features, or whether the parasites themselves induce a higher bacterial richness.

SUBMITTER: Mondot S

PROVIDER: S-EPMC8417078 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundInvertebrates are a very attractive subject for studying host-microbe interactions because of their simple gut microbial community and host diversity. Studying the composition of invertebrate gut microbiota and the determining factors is essential for understanding their symbiotic mechanism. Cephalopods are invertebrates that have similar biological properties to vertebrates such as closed circulation system, an advanced nervous system, and a well-differentiated digestive system. However, it is not currently known whether their microbiomes have more in common with vertebrates or invertebrates. This study reports on the microbial composition of six cephalopod species and compares them with other mollusk and marine fish microbiomes to investigate the factors that shape the gut microbiota.ResultsEach cephalopod gut consisted of a distinct consortium of microbes, with Photobacterium and Mycoplasma identified as core taxa. The gut microbial composition of cephalopod reflected their host phylogeny, the importance of which was supported by a detailed oligotype-level analysis of operational taxonomic units assigned to Photobacterium and Mycoplasma. Photobacterium typically inhabited multiple hosts, whereas Mycoplasma tended to show host-specific colonization. Furthermore, we showed that class Cephalopoda has a distinct gut microbial community from those of other mollusk groups or marine fish. We also showed that the gut microbiota of phylum Mollusca was determined by host phylogeny, habitat, and diet.ConclusionWe have provided the first comparative analysis of cephalopod and mollusk gut microbial communities. The gut microbial community of cephalopods is composed of distinctive microbes and is strongly associated with their phylogeny. The Photobacterium and Mycoplasma genera are core taxa within the cephalopod gut microbiota. Collectively, our findings provide evidence that cephalopod and mollusk gut microbiomes reflect host phylogeny, habitat, and diet. It is hoped that these data can contribute to future studies on invertebrate-microbe interactions.

Project description:Host-parasite interactions may be modulated by host- or parasite-associated microbes, but the role of these are often overlooked. Particularly for parasites with intestinal stages (either larval or adult), the host gut microbiome may play a key role for parasite establishment; moreover, the microbiome may change in response to invading parasites. Hypothesis testing at the organismal level may be hampered, particularly in mammalian definitive hosts, by ethical, logistical, and economical restrictions. Thus, invertebrates naturally serving as intermediate hosts to parasites with complex life cycles may inform the development of mammalian models as an early-stage host-parasite model. In addition, several important pathogens are vectored by insects, and insect gut microbiome-pathogen interactions may provide essential base-line knowledge, which may be used to control vectorborne pathogens. Here, we used the grain beetle, Tenebrio molitor, a host of the tapeworm Hymenolepis diminuta, to explore interactions between infection status and resident gut microbiota at two pre-determined time points (day two and seven) post infection. Using 16S/18S microbial profiling, we measured key parameters of the composition, relative abundance, and diversity of the host gut bacteriome and mycobiome. In addition, we quantified the systemic beetle immune response to infection by Phenoloxidase activity and hemocyte abundance. We found significant changes in the gut bacteriome and mycobiome in relation to infection status and beetle age. Thus, the relative abundance of Proteobacteria was significantly higher in the gut of infected beetles and driven mostly by an increased abundance of Acinetobacter. In addition, the mycobiome was less abundant in infected beetles but maintained higher Shannon diversity in infected compared with non-infected beetles. Beetles treated with a broad-spectrum antibiotic (Tetracycline) exhibited significantly reduced parasite establishment compared with the untreated control group, indicating that the host microbiome may greatly influence hatching of eggs and subsequent establishment of H. diminuta larvae. Our results suggest that experimental work using invertebrates may provide a platform for explorative studies of host-parasite-microbe interactions and their underlying mechanisms.

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Parasites and diet as main drivers of the Malagasy gut microbiome richness and function.

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