Prevotella copri and its related taxa are widely detected in mammalian gut microbiomes and have been linked with an enterotype in humans. However, their microevolution and macroevolution among hosts are poorly characterized. In this study, extensively collected marker genes and genomes were analyzed to trace their evolutionary history, host specificity, and biogeographic distribution. Investigations based on marker genes and genomes suggest that a P. copri-containing lineage (PCL) harbors diverse species in higher primates. Firstly, P. copri in the human gut consisted of multiple groups exhibiting high genomic divergence and conspicuous but non-strict biogeographic patterns. Most African strains with high genomic divergence from other strains were phylogenetically located at the root of the species, indicating the co-evolutionary history of P. copri and Homo sapiens. Secondly, although long-term co-evolution between PCL and higher primates was revealed, sporadic signals of co-speciation and extensive host jumping of PCL members were suggested among higher primates. Metagenomic and phylogenetic analyses indicated that P. copri and other PCL species found in domesticated mammals had been recently transmitted from humans. Thirdly, strong evidence was found on the extensively horizontal transfer of genes (e.g., genes encoding carbohydrate-active enzymes) among sympatric P. copri groups and PCL species in the same primate host. Our study provides panoramic insights into the combined effects of vertical and horizontal transmission, as well as potential niche adaptation, on the microevolutionary and macroevolutionary history for an enterotype-representative lineage.

Prevotella copri and related taxa are widely detected in mammalian gut microbiomes and have been linked with one human enterotype. However, their microevolution and macroevolution among hosts are poorly characterized. In this study, extensively collected marker genes and genomes were analyzed to trace their evolutionary history, host specificity, and biogeographic distribution. Investigations based on 16S rRNA gene, gyrB, and genomes suggested that a multi-specific P. copri-containing lineage (PCL) harbors diverse species in higher primates. Firstly, P. copri is the dominant species of PCL in the human gut and consists of multiple groups exhibiting high genomic divergence and conspicuous but non-strict biogeographic pattern. Most African strains with high genomic divergence from other strains were phylogenetically placed near the species root, indicating the co-evolutionary history of P. copri and Homo sapiens. Secondly, although long-term co-evolution between PCL and higher primates was revealed, sporadic signals of co-speciation and extensive host jumping of PCL members were observed among higher primates. Metagenomic and phylogenetic analyses indicated that P. copri and other PCL species found in captive mammals have been recently transmitted from humans. Thirdly, strong evidence was found on the extensively horizontal transfer of genes (e.g., carbohydrate-active enzyme encoding genes) among sympatric P. copri groups and PCL species in the same primate host. Our study provides panoramic insights into the complex effects of vertical and horizontal transmission, and potential niche adaption on speciation, host, and biogeographical distribution spanning microevolutionary and macroevolutionary history for a certain gut bacterial lineage.ImportancePrevotella copri and its related taxa, which we designated as Prevotella copri-containing lineage (PCL) in the present study, are widely detected in guts of human, non-human primates and many captive mammals, showing positive or negative correlation to some human diseases. However, a comprehensive understanding on its microevolutionary (within P. copri) and macroevolutionary (among PCL members) history across host species and host biogeography is still lacking. According to our analysis based on 16S rRNA gene, gyrB and genomes, we provided the panoramic insights into the putative effects of vertical transfer, horizontal transmission and potential niche selection on host and biogeographical distribution of this gut bacterial lineage and P. copri. To our knowledge, it is the first time that a gut bacterial lineage was studied at both micro- and macroevolutionary levels, which can aid our systematic understanding on the host-microbe co-evolutionary interactions.