Insect guts present distinctive environments for microbial colonization, and bacteria in the gut potentially provide many beneficial services to their hosts. Insects display a wide range in degree of dependence on gut bacteria for basic functions. Most insect guts contain relatively few microbial species as compared to mammalian guts, but some insects harbor large gut communities of specialized bacteria. Others are colonized only opportunistically and sparsely by bacteria common in other environments. Insect digestive tracts vary extensively in morphology and physicochemical properties, factors that greatly influence microbial community structure. One obstacle to the evolution of intimate associations with gut microorganisms is the lack of dependable transmission routes between host individuals. Here, social insects, such as termites, ants, and bees, are exceptions: social interactions provide opportunities for transfer of gut bacteria, and some of the most distinctive and consistent gut communities, with specialized beneficial functions in nutrition and protection, have been found in social insect species. Still, gut bacteria of other insects have also been shown to contribute to nutrition, protection from parasites and pathogens, modulation of immune responses, and communication. The extent of these roles is still unclear and awaits further studies.

The gut microbiota of insects - diversity in structure and function.

In this Analysis we use published 16S ribosomal RNA gene sequences to compare the bacterial assemblages that are associated with humans and other mammals, metazoa and free-living microbial communities that span a range of environments. The composition of the vertebrate gut microbiota is influenced by diet, host morphology and phylogeny, and in this respect the human gut bacterial community is typical of an omnivorous primate. However, the vertebrate gut microbiota is different from free-living communities that are not associated with animal body habitats. We propose that the recently initiated international Human Microbiome Project should strive to include a broad representation of humans, as well as other mammalian and environmental samples, as comparative analyses of microbiotas and their microbiomes are a powerful way to explore the evolutionary history of the biosphere.

Worlds within worlds: evolution of the vertebrate gut microbiota

Alkaline pH homeostasis in bacteria: new insights.

Drosophila melanogaster is emerging as an important model of non-pathogenic host–microbe interactions. The genetic and experimental tractability of Drosophila has led to significant gains in our understanding of animal–microbial symbiosis. However, the full implications of these results cannot be appreciated without the knowledge of the microbial communities associated with natural Drosophila populations. In particular, it is not clear whether laboratory cultures can serve as an accurate model of host–microbe interactions that occur in the wild, or those that have occurred over evolutionary time. To fill this gap, we characterized natural bacterial communities associated with 14 species of Drosophila and related genera collected from distant geographic locations. To represent the ecological diversity of Drosophilids, examined species included fruit-, flower-, mushroom-, and cactus-feeders. In parallel, wild host populations were compared to laboratory strains, and controlled experiments were performed to assess the importance of host species and diet in shaping bacterial microbiome composition. We find that Drosophilid flies have taxonomically restricted bacterial communities, with 85% of the natural bacterial microbiome composed of only four bacterial families. The dominant bacterial taxa are widespread and found in many different host species despite the taxonomic, ecological, and geographic diversity of their hosts. Both natural surveys and laboratory experiments indicate that host diet plays a major role in shaping the Drosophila bacterial microbiome. Despite this, the internal bacterial microbiome represents only a highly reduced subset of the external bacterial communities, suggesting that the host exercises some level of control over the bacteria that inhabit its digestive tract. Finally, we show that laboratory strains provide only a limited model of natural host–microbe interactions. Bacterial taxa used in experimental studies are rare or absent in wild Drosophila populations, while the most abundant associates of natural Drosophila populations are rare in the lab.

https://escholarship.org/content/qt7343441k/qt7343441k.pdf?t=qajnct

Bacterial communities of diverse Drosophila species: ecological context of a host-microbe model system.

Background: Greenhouse gas (GHG) production, as a cause of climate change, is considered as one of the biggest problems society is currently facing. The livestock sector is one of the large contributors of anthropogenic GHG emissions. Also, large amounts of ammonia (NH3), leading to soil nitrification and acidification, are produced by livestock. Therefore other sources of animal protein, like edible insects, are currently being considered. Methodology/Principal Findings: An experiment was conducted to quantify production of carbon dioxide (CO2) and average daily gain (ADG) as a measure of feed conversion efficiency, and to quantify the production of the greenhouse gases methane (CH4) and nitrous oxide (N2O) as well as NH3 by five insect species of which the first three are considered edible: Tenebrio molitor, Acheta domesticus, Locusta migratoria, Pachnoda marginata, and Blaptica dubia. Large differences were found among the species regarding their production of CO2 and GHGs. The insects in this study had a higher relative growth rate and emitted comparable or lower amounts of GHG than described in literature for pigs and much lower amounts of GHG than cattle. The same was true for CO2 production per kg of metabolic weight and per kg of mass gain. Furthermore, also the production of NH3 by insects was lower than for conventional livestock. Conclusions/Significance: This study therefore indicates that insects could serve as a more environmentally friendly alternative for the production of animal protein with respect to GHG and NH3 emissions. The results of this study can be used as basic information to compare the production of insects with conventional livestock by means of a life cycle analysis.

/pdf/an-exploration-on-greenhouse-gas-and-ammonia-production-by-37c0vu3zw7.pdf

An exploration on greenhouse gas and ammonia production by insect species suitable for animal or human consumption.

The guts of soil-feeding macroinvertebrates contain a complex microbial community that is involved in the transformation of ingested soil organic matter. In a companion paper (T. Lemke, U. Stingl, M. Egert, M. W. Friedrich, and A. Brune, Appl. Environ. Microbiol. 69:6650-6658, 2003), we show that the gut of our model organism, the humivorous larva of the cetoniid beetle Pachnoda ephippiata, is characterized by strong midgut alkalinity, high concentrations of microbial fermentation products, and the presence of a diverse, yet unstudied microbial community. Here, we report on the community structure of bacteria and archaea in the midgut, hindgut, and food soil of P. ephippiata larvae, determined with cultivation-independent techniques. Clone libraries and terminal restriction fragment length polymorphism analysis of 16S rRNA genes revealed that the intestines of P. ephippiata larvae contain a complex gut microbiota that differs markedly between midgut and hindgut and that is clearly distinct from the microbiota in the food soil. The bacterial community is dominated by phylogenetic groups with a fermentative metabolism (Lactobacillales, Clostridiales, Bacillales, and Cytophaga-Flavobacterium-Bacteroides [CFB] phylum), which is corroborated by high lactate and acetate concentrations in the midgut and hindgut and by the large numbers of lactogenic and acetogenic bacteria in both gut compartments reported in the companion paper. Based on 16S rRNA gene frequencies, Actinobacteria dominate the alkaline midgut, while the hindgut is dominated by members of the CFB phylum. The archaeal community, however, is less diverse. 16S rRNA genes affiliated with mesophilic Crenarchaeota, probably stemming from the ingested soil, were most frequent in the midgut, whereas Methanobacteriaceae-related 16S rRNA genes were most frequent in the hindgut. These findings agree with the reported restriction of methanogenesis to the hindgut of Pachnoda larvae.

Microbial community structure in midgut and hindgut of the humus-feeding larva of Pachnoda ephippiata (Coleoptera: Scarabaeidae).

The soil macrofauna plays an important role in the carbon and nitrogen cycle of terrestrial ecosystems (18, 41, 62). The intestinal tracts of litter-feeding and humivorous soil macroinvertebrates are favorable habitats for microorganisms and typically harbor a dense and active gut microbiota. The major function commonly attributed to the microorganisms in the guts of such animals is the depolymerization and fermentative breakdown of the cellulosic or lignocellulosic component of their diet, which leads to degradation products that can be resorbed by the host. This is supported by the high concentrations of microbial fermentation products and by the presence of fermentative bacteria and protozoa, accompanied by obligately anaerobic homoacetogenic and methanogenic microorganisms, in the guts of such animals. However, the extent and importance of such processes and their specific function in the nutrition of the host are scarcely understood (for reviews, see references 8, 9, 11, 12, 14, 36, and 44).

In the case of soil-feeding termites, host factors such as the extreme alkalinity of the anterior hindgut and the influx of oxygen seem to play a key role in sequestering organic matter from the inorganic soil matrix (37). The decrease of molecular weight and increase in solubility resulting from alkaline extraction and chemical oxidation render the organic matter accessible for digestion in subsequent, less-alkaline compartments (34, 35). Alkaline gut regions are encountered also in many representatives of other insect orders and seem to be connected with the dietary preferences of the respective taxa (Coleoptera, Diptera, and Lepidoptera; see references 15 and 32). Comparing several beetle larvae feeding on a lignocellulosic diet, Grayson (30) already had pointed out an apparent correlation between the degree of humification of the diet and the alkalinity of the intestinal tract. The highest pH values among beetle larvae were encountered among the Scarabaeidae (50, 52, 58, 60), which comprise species from humivorous, detritivorous, and coprophagous feeding guilds. Although scarab beetle larvae are among those few arthropods that have received at least a minimum of attention from a microbiological perspective (3, 4, 21, 23) and although their importance for the transformation of soil organic matter is undisputed, little is known about the composition of the gut microbial community and its role in the digestive process.

Using the humivorous larva of the cetoniid beetle Pachnoda ephippiata (Coleoptera: Scarabaeidae) as a model organism, we investigated the physicochemical conditions and microbial activities in the gut in order to gain more insight into the role of the intestinal microbiota in transformation and mineralization of organic matter during gut passage. Since a representative analysis of the microbial community structure requires covering also those populations that resist cultivation (14), the project also included a cultivation-independent approach, involving molecular cloning and fingerprinting techniques. These results are reported and discussed in the companion paper (28).

Physicochemical conditions and microbial activities in the highly alkaline gut of the humus-feeding larva of Pachnoda ephippiata (Coleoptera: Scarabaeidae).

In the intestinal tracts of animals, methanogenesis from CO(2) and other C(1) compounds strictly depends on the supply of electron donors by fermenting bacteria, but sources and sinks of reducing equivalents may be spatially separated. Microsensor measurements in the intestinal tract of the omnivorous cockroach Blaberus sp. showed that molecular hydrogen strongly accumulated in the midgut (H(2) partial pressures of 3 to 26 kPa), whereas it was not detectable (<0.1 kPa) in the posterior hindgut. Moreover, living cockroaches emitted large quantities of CH(4) [105 +/- 49 nmol (g of cockroach)(-1) h(-1)] but only traces of H(2). In vitro incubation of isolated gut compartments, however, revealed that the midguts produced considerable amounts of H(2), whereas hindguts emitted only CH(4) [106 +/- 58 and 71 +/- 50 nmol (g of cockroach)(-1) h(-1), respectively]. When ligated midgut and hindgut segments were incubated in the same vials, methane emission increased by 28% over that of isolated hindguts, whereas only traces of H(2) accumulated in the headspace. Radial hydrogen profiles obtained under air enriched with H(2) (20 kPa) identified the hindgut as an efficient sink for externally supplied H(2). A cross-epithelial transfer of hydrogen from the midgut to the hindgut compartment was clearly evidenced by the steep H(2) concentration gradients which developed when ligated fragments of midgut and hindgut were placed on top of each other-a configuration that simulates the situation in vivo. These findings emphasize that it is essential to analyze the compartmentalization of the gut and the spatial organization of its microbiota in order to understand the functional interactions among different microbial populations during digestion.

Thorsten Lemke

Papers

Microbial community structure in midgut and hindgut of the humus-feeding larva of Pachnoda ephippiata (Coleoptera: Scarabaeidae).

Physicochemical conditions and microbial activities in the highly alkaline gut of the humus-feeding larva of Pachnoda ephippiata (Coleoptera: Scarabaeidae).

Cross-Epithelial Hydrogen Transfer from the Midgut Compartment Drives Methanogenesis in the Hindgut of Cockroaches