Disentangling the Relative Roles of Vertical Transmission, Subsequent Colonizations, and Diet on Cockroach Microbiome Assembly.

A multitude of factors affect the assemblies of complex microbial communities associated with animal hosts, with implications for community flexibility, resilience, and long-term stability; however, their relative effects have rarely been deduced. Here, we use a tractable lab model to quantify the relative and combined effects of parental transmission (egg case microbiome present/reduced), gut inocula (cockroach versus termite gut provisioned), and varying diets (matched or unmatched with gut inoculum source) on gut microbiota structure of hatchlings of the omnivorous cockroach Shelfordella lateralis using 16S rRNA gene (rDNA) amplicon sequencing. We show that the presence of a preexisting bacterial community via vertical transmission of microbes on egg cases reduces subsequent microbial invasion, suggesting priority effects that allow initial colonizers to take a strong hold and which stabilize the microbiome. However, subsequent inoculation sources more strongly affect ultimate community composition and their ecological networks, with distinct host-taxon-of-origin effects on which bacteria establish. While this is so, communities respond flexibly to specific diets in ways that consequently impact predicted community functions. In conclusion, our findings suggest that inoculations drive communities toward different stable states depending on colonization and extinction events, through ecological host-microbe relations and interactions with other gut bacteria, while diet in parallel shapes the functional capabilities of these microbiomes. These effects may lead to consistent microbial communities that maximize the extended phenotype that the microbiota provides the host, particularly if microbes spend most of their lives in host-associated environments.IMPORTANCE When host fitness is dependent on gut microbiota, microbial community flexibility and reproducibility enhance host fitness by allowing fine-tuned environmental tracking and sufficient stability for host traits to evolve. Our findings lend support to the importance of vertically transmitted early-life microbiota as stabilizers, through interactions with potential colonizers, which may contribute to ensuring that the microbiota aligns within host fitness-enhancing parameters. Subsequent colonizations are driven by microbial composition of the sources available, and we confirm that host-taxon-of-origin affects stable subsequent communities, while communities at the same time retain sufficient flexibility to shift in response to available diets. Microbiome structure is thus the result of the relative impact and combined effects of inocula and fluctuations driven by environment-specific microbial sources and digestive needs. These affect short-term community structure on an ecological time scale but could ultimately shape host species specificities in microbiomes across evolutionary time, if environmental conditions prevail.

Renelies-Hamilton J ，Germer K ，Sillam-Dussès D ，Bodawatta KH ，Poulsen M ... -  《mSphere》

Phylosymbiosis across Deeply Diverging Lineages of Omnivorous Cockroaches (Order Blattodea).

The gut microbiome is shaped by both host diet and host phylogeny. However, separating the relative influence of these two factors over long periods of evolutionary time is often difficult. We conducted a 16S rRNA gene amplicon-based survey of the gut microbiome from 237 individuals and 19 species of omnivorous cockroaches from the order Blattodea. The order Blattodea represents an ancient lineage of insects that emerged over 300 million years ago, have a diverse gut microbiota, and have a typically gregarious lifestyle. All cockroaches shared a broadly similar gut microbiota, with 66 microbial families present across all species and 13 present in every individual examined. Although our network analysis of the cockroach gut microbiome showed a large amount of connectivity, we demonstrated that gut microbiota cluster strongly by host species. We conducted follow-up tests to determine if cockroaches exhibit phylosymbiosis, or the tendency of host-associated microbial communities to parallel the phylogeny of related host species. Across the full data set, gut microbial community similarity was not found to correlate with host phylogenetic distance. However, a weak but significant phylosymbiotic signature was observed using the matching cluster metric, which allows for localized changes within a phylogenetic tree that are more likely to occur over long evolutionary distances. This finding suggests that host phylogeny plays a large role in structuring the cockroach gut microbiome over shorter evolutionary distances and a weak but significant role in shaping the gut microbiome over extended periods of evolutionary time.IMPORTANCE The gut microbiome plays a key role in host health. Therefore, it is important to understand the evolution of the gut microbiota and how it impacts, and is impacted by, host evolution. In this study, we explore the relationship between host phylogeny and gut microbiome composition in omnivorous, gregarious cockroaches within the Blattodea order, an ancient lineage that spans 300 million years of evolutionary divergence. We demonstrate a strong relationship between host species identity and gut microbiome composition and found a weaker but significant role for host phylogeny in determining microbiome similarity over extended periods of evolutionary time. This study advances our understanding of the role of host phylogeny in shaping the gut microbiome over different evolutionary distances.

Tinker KA ，Ottesen EA 《-》

The Core Gut Microbiome of the American Cockroach, Periplaneta americana, Is Stable and Resilient to Dietary Shifts.

The omnivorous cockroach Periplaneta americana hosts a diverse hindgut microbiota encompassing hundreds of microbial species. In this study, we used 16S rRNA gene sequencing to examine the effect of diet on the composition of the P. americana hindgut microbial community. Results show that the hindgut microbiota of P. americana exhibit a highly stable core microbial community with low variance in compositions between individuals and minimal community change in response to dietary shifts. This core hindgut microbiome is shared between laboratory-hosted and wild-caught individuals, although wild-caught specimens exhibited a higher diversity of low-abundance microbes that were lost following extended cultivation under laboratory conditions. This taxonomic stability strongly contrasts with observations of the gut microbiota of mammals, which have been shown to be highly responsive to dietary change. A comparison of P. americana hindgut samples with human fecal samples indicated that the cockroach hindgut community exhibited higher alpha diversity but a substantially lower beta diversity than the human gut microbiome. This suggests that cockroaches have evolved unique mechanisms for establishing and maintaining a diverse and stable core microbiome. The gut microbiome plays an important role in the overall health of its host. A healthy gut microbiota typically assists with defense against pathogens and the digestion and absorption of nutrients from food, while dysbiosis of the gut microbiota has been associated with reduced health. In this study, we examined the composition and stability of the gut microbiota from the omnivorous cockroach Periplaneta americana. We found that P. americana hosts a diverse core gut microbiome that remains stable after drastic long-term changes in diet. While other insects, notably ant and bee species, have evolved mechanisms for maintaining a stable association with specific gut microbiota, these insects typically host low-diversity gut microbiomes and consume specialized diets. In contrast, P. americana hosts a gut microbiota that is highly species rich and consumes a diverse solid diet, suggesting that cockroaches have evolved unique mechanisms for developing and maintaining a stable gut microbiota.

Tinker KA ，Ottesen EA 《-》

Overlapping Community Compositions of Gut and Fecal Microbiomes in Lab-Reared and Field-Collected German Cockroaches.

German cockroaches, Blattella germanica (Blattodea: Ectobiidae), are human commensals that move freely between food and waste, disseminating bacteria, including potential pathogens, through their feces. However, the relationship between the microbial communities of the cockroach gut and feces is poorly understood. We analyzed the V4 region of the 16S rRNA gene and the V9 region of the 18S rRNA gene by next-generation sequencing (NGS) to compare the bacterial and protist diversities in guts versus feces and males versus females, as well as assess variation across cockroach populations. Cockroaches harbored a diverse array of bacteria, and 80 to 90% of the operational taxonomic units (OTUs) were shared between the feces and gut. Lab-reared and field-collected cockroaches had distinct microbiota, and whereas lab-reared cockroaches had relatively conserved communities, considerable variation was observed in the microbial community composition of cockroaches collected in different apartments. Nonetheless, cockroaches from all locations shared some core bacterial taxa. The eukaryotic community in the feces of field-collected cockroaches was found to be more diverse than that in lab-reared cockroaches. These results demonstrate that cockroaches disseminate their gut microbiome in their feces, and they underscore the important contribution of the cockroach fecal microbiome to the microbial diversity of cockroach-infested homes.IMPORTANCE The German cockroach infests diverse human-built structures, including homes and hospitals. It produces potent allergens that trigger asthma and disseminates opportunistic pathogens in its feces. A comprehensive understanding of gut and fecal microbial communities of cockroaches is essential not only to understand their contribution to the biology of the cockroach, but also for exploring their clinical relevance. In this study, we compare the diversity of bacteria and eukaryotes in the cockroach gut and feces and assess the variation in the gut microbiota across cockroach populations.

Kakumanu ML ，Maritz JM ，Carlton JM ，Schal C ... -  《-》

Seasonal Dietary Shifts Alter the Gut Microbiota of Avivorous Bats: Implication for Adaptation to Energy Harvest and Nutritional Utilization.

Gong L ，Liu B ，Wu H ，Feng J ，Jiang T ... -  《mSphere》