Genomes of Gut Bacteria from Nasonia Wasps Shed Light on Phylosymbiosis and Microbe-Assisted Hybrid Breakdown

Abstract

Phylosymbiosis is a cross-system trend whereby microbial community relationships recapitulate the host phylogeny. In Nasonia parasitoid wasps, phylosymbiosis occurs throughout development, is distinguishable between sexes, and benefits host development and survival. Moreover, the microbiome shifts in hybrids as a rare Proteus bacterium in the microbiome becomes dominant. The larval hybrids then catastrophically succumb to bacterium-assisted lethality and reproductive isolation between the species. Two important questions for understanding phylosymbiosis and bacterium-assisted lethality in hybrids are (i) do the Nasonia bacterial genomes differ from other animal isolates and (ii) are the hybrid bacterial genomes the same as those in the parental species? Here, we report the cultivation, whole-genome sequencing, and comparative analyses of the most abundant gut bacteria in Nasonia larvae, Providencia rettgeri and Proteus mirabilis. Characterization of new isolates shows Proteus mirabilis forms a more robust biofilm than Providencia rettgeri and that, when grown in coculture, Proteus mirabilis significantly outcompetes Providencia rettgeri. Providencia rettgeri genomes from Nasonia are similar to each other and more divergent from pathogenic, human associates. Proteus mirabilis from Nasonia vitripennis, Nasonia giraulti, and their hybrid offspring are nearly identical and relatively distinct from human isolates. These results indicate that members of the larval gut microbiome within Nasonia are most similar to each other, and the strain of the dominant Proteus mirabilis in hybrids is resident in parental species. Holobiont interactions between shared, resident members of the wasp microbiome and the host underpin phylosymbiosis and hybrid breakdown. IMPORTANCE Animal and plant hosts often establish intimate relationships with their microbiomes. In varied environments, closely related host species share more similar microbiomes, a pattern termed phylosymbiosis. When phylosymbiosis is functionally significant and beneficial, microbial transplants between host species and host hybridization can have detrimental consequences on host biology. In the Nasonia parasitoid wasp genus, which contains a phylosymbiotic gut community, both effects occur and provide evidence for selective pressures on the holobiont. Here, we show that bacterial genomes in Nasonia differ from other environments and harbor genes with unique functions that may regulate phylosymbiotic relationships. Furthermore, the bacteria in hybrids are identical to those in parental species, thus supporting a hologenomic tenet that the same members of the microbiome and the host genome impact phylosymbiosis, hybrid breakdown, and speciation.

Strain-Level Variation and Diverse Host Bacterial Responses in Episymbiotic Saccharibacteria

“…Each of the HMT-352 strains shared a majority of its genome with all other studied HMT-352 strains, with approximately 70% of the genes in each genome being core to all HMT-352 strains. This proportion is similar to that of other studied bacterial species, although the proportion can vary substantially based on both the number of genome representatives and the degree of gene flow ( 37 – 39 ). However, despite the predicted homology for such large portions of the genome, the nucleotide sequences of the homologous regions differed substantially, resulting in ANI values between 93% and 95%.…”

Lipopolysaccharide -mediated resistance to host antimicrobial peptides and hemocyte-derived reactive-oxygen species are the major Providencia alcalifaciens virulence factors in Drosophila melanogaster

“…melanogaster [ 41 ] and in the guts and external environment of D . melanogaster [ 42 , 43 ] but they have also been found in various other insects such as medicinal maggots [ 44 ], stable flies [ 45 ], Mexican fruit flies [ 46 ], house flies [ 47 ], mediterranean fruit fly [ 48 ], Nasonia wasps [ 49 ], black soldier fly [ 50 ], olive fly [ 51 ].…”

The Phylosymbiosis Pattern Between the Fig Wasps of the Same Genus and Their Associated Microbiota

“…For instance, transplanting interspecific microbial communities in Peromyscus deer mice significantly decreased their ability to digest food, and Nasonia wasps that received transplants of microbial communities from different wasp species had lower survival rate than those given their own microbiota ( Brooks et al, 2016 ). In Nasonia parasitoid wasps, the microbiome shifts in hybrids, as a rare Proteus bacteria become dominant, so the larval hybrids then catastrophically succumb to bacterium-assisted lethality and reproductive isolation between the species ( Cross et al, 2021 ). All these data showed that host characteristics could regulate microbial communities, and changes in the microbial communities were involved in host hybridization lethality, which reflected a mutually restrictive coevolutionary relationship between the hosts and associated microbiota.…”