Abstract
Insect gut microbes have been shown to provide nutrients such as essential amino acids (EAAs) to their hosts. How this symbiotic nutrient provisioning tracks with the host’s demand is not well understood. In this study, we investigated microbial essential amino acid (EAA) provisioning in omnivorous American cockroaches (Periplaneta americana), fed low-quality (LQD) and comparatively higher-quality dog food (DF) diets using carbon stable isotope ratios of EAAs (δ13CEAA). We assessed non-dietary EAA input, quantified as isotopic offsets (Δ13C) between cockroach (δ13CCockroach EAA) and dietary (δ13CDietary EAA) EAAs, and subsequently determined biosynthetic origins of non-dietary EAAs in cockroaches using 13C-fingerprinting with dietary and representative bacterial and fungal δ13CEAA. Investigation of biosynthetic origins of de novo non-dietary EAAs indicated bacterial origins of EAA in cockroach appendage samples, and a mixture of fungal and bacterial EAA origins in gut filtrate samples for both LQD and DF-fed groups. We attribute the bacteria-derived EAAs in cockroach appendages to provisioning by the fat body residing obligate endosymbiont, Blattabacterium and gut-residing bacteria. The mixed signatures of gut filtrate samples are attributed to the presence of unassimilated dietary, as well as gut microbial (bacterial and fungal) EAAs. This study highlights the potential impacts of dietary quality on symbiotic EAA provisioning and the need for further studies investigating the interplay between host EAA demands, host dietary quality and symbiotic EAA provisioning in response to dietary sufficiency or deficiency.
Highlights
Insects persisting on diets limited in essential nutrients are posited to rely on mutualistic symbiosis with microbes to acquire these nutrients and meet requirements for growth, fecundity, longevity and fitness (Douglas, 2009)
We uncovered symbiotic essential amino acids (EAAs) inputs in both Low-quality diet (LQD)-fed and dog food (DF)-fed P. americana cockroaches under controlled-feeding conditions using δ13CEAA analyses, EAA provisioning was comparatively higher in the DF-fed cockroaches, contrary to our hypothesis
We make no distinction between EAA provisioning by gut microbes or the fat body-residing obligate symbiont Blattabacterium since we did not use Blattabacterium-free cockroaches
Summary
Insects persisting on diets limited in essential nutrients are posited to rely on mutualistic symbiosis (obligate or facultative) with microbes to acquire these nutrients and meet requirements for growth, fecundity, longevity and fitness (Douglas, 2009). Microbial species diversity and the complexity of interspecies interactions in the guts of insect hosts make ascertaining the contributions and functions of gut-associated microbiota challenging. This difficulty is further compounded by considerable variations in community composition with time and host developmental stages, as well as differences in physicochemical requirements (oxygen and pH) needed by community members in order to perform particular functions (Engel & Moran, 2013). No difference in community composition was detected in cockroaches fed a high or low fiber diet (Schauer, Thompson & Brune, 2014) The implications of these diet-induced effects on microbiota composition and functions, such as EAA provisioning remain unclear
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