Gut bacteria mediate aggregation in the German cockroach

Wada‐Katsumata, Ayako; Zurek, Ludek; Nalyanya, Godfrey; Roelofs, Wendell L.; Zhang, Aijun; Schal, Coby

doi:10.1073/pnas.1504031112

Cited by 159 publications

(120 citation statements)

References 58 publications

(28 reference statements)

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“…While this is not thought to be an obligate symbiosis, reducing the gut microbiota in Periplaneta americana slows development and results in lowered body weight and metabolic activity, suggesting that the gut microbiota plays an important role in the health and fitness of cockroaches (7)(8)(9). Recent work also suggested that the hindgut microbiota is responsible for producing pheromones, including volatile fatty acids, which promote social behavior among cockroaches (10).…”

mentioning

confidence: 99%

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

Tinker

Ottesen

2016

Appl Environ Microbiol

111

131

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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. IMPORTANCEThe 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. Most insects host simple gut microbial communities, with only a few unique species represented; the reed beetle, honey bee, fruit fly, and gypsy moth all have fewer than 10 species of bacteria in their guts (1). The low complexity of these communities has been attributed to selective pressures dictated by host physiology (2) and the lack of extensive parental contact with offspring in many insects, which offers few opportunities for vertical and social transmission of gut microbes (1, 3). However, certain social and/or gregarious insect species, including cockroaches and their close relatives, the termites, host complex gut communities comprising hundreds of species (1,4,5).The cockroach gut is composed of three compartments: the foregut, midgut, and hindgut. Of the three, ...

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mentioning

confidence: 99%

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

Tinker

Ottesen

2016

Appl Environ Microbiol

111

131

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“…This possibility is supported by recent findings that gut bacteria mediate aggregations of German cockroaches. 15 The gut bacterial community of German cockroaches emits highly volatile carboxylic acids that, in turn, elicit the aggregation behavior of its insect host. Whether the microbial gut flora of bed bugs is capable of producing the bed bug pheromone components DMDS and DMTS is not yet known, but various microorganisms possess a methionine gamma lyase which degrades L-methionine directly to methanthiol which is then converted to DMDS and DMTS.…”

Section: Discussionmentioning

confidence: 99%

Common bed bugs can biosynthesize pheromone components from amino acid precursors in human blood

et al. 2018

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We have recently shown that the aggregation pheromone of the common bed bug, Cimex lectularius, comprises a six-component blend of dimethyl disulfide (DMDS), dimethyl trisulfide (DMTS), (E)-2-hexenal, (E)-2-octenal, 2-hexanone, and histamine. Here, we tested the hypothesis that bed bugs biosynthesize some pheromone components from amino acid precursors in human blood, namely DMDS and DMTS from L-methionine and histamine from histidine. We tested this hypothesis by (i) allowing bed bugs to feed on and metabolize sheep blood enriched with 13C-labelled histidine or 2H-labelled methionine, (ii) extracting bed bug feces (a source of the aggregation pheromone), and (iii) analyzing feces extracts by GC-MS, HPLC-MS and NMR spectroscopy. The analyses revealed that bed bugs converted 2H-methionine to 2H-DMDS and 2H-DMTS, and 13C-histidine to 13C-histamine. There is not enough histidine in human blood to account for the amount of histamine that bed bugs produce and excrete with their feces, and only a small proportion of the available 13C-histidine was converted to 13C-histamine in our study. Therefore, it is likely that bed bugs biosynthesize histamine, and possibly also DMDS and DMTS, primarily de novo.

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“…Bacteria in cockroach guts display tremendous phylogenetic diversity, and include members of Bacteroidetes, Firmicutes, Fibrobacteres, and Proteobacteria (Dietrich et al, 2014;Mikaelyan et al, 2015b). The assemblage is dominated by obligate anaerobes, including those that break down structural polysaccharides of plant-based detritus (Bignell, 1977;Cruden and Markovetz, 1979, 1984, produce semiochemicals that influence host social behavior (Wada-Katsumata et al, 2015) and directly affect development by regulating gene expression in their host (Cruden and Markovetz, 1987;Jahnes et al, 2019). Another advantage of trophallaxis is that metabolic products of the parents and their resident microbial assemblage would not be compromised by exposure to the outside environment; these include hormones, enzymes, metabolites, and other chemicals that may serve as physiological or behavioral signals.…”

Section: Host Fitness Benefitsmentioning

confidence: 99%

Origin of Mutualism Between Termites and Flagellated Gut Protists: Transition From Horizontal to Vertical Transmission

Nalepa

2020

Front. Ecol. Evol.

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Lower termites, as well as their sister group, the subsocial wood-feeding cockroach Cryptocercus, rely on flagellated eukaryotic symbionts in the hindgut to cooperatively digest their wood diet. In Cryptocercus these flagellates undergo encystment cycles tightly coordinated with the molting cycle of their host, yet the resultant cysts play no demonstrated role in their transmission to neonates; the trophozoite stage of the flagellates is passed directly from parents to offspring via hindgut fluids (proctodeal trophallaxis). This pattern suggests that encystment is a vestige from a gregarious cockroach ancestor, when the flagellates had a functional, two-stage life cycle and the cysts were horizontally transmitted among hosts via coprophagy. The strong integration between flagellate encystment cycles and host developmental physiology in Cryptocercus indicates that the relationship of the flagellates with their proposed gregarious cockroach ancestor was not commensal, but parasitic, with flagellates likely obtaining benefits by taking advantage of host gut metabolites and ingested plant debris. When vertical transmission evolved the parasites were 'captured,' and their fitness became inescapably embedded in the fitness of their host. The vertical transmission of gut flagellates and the origin of host subsociality via proctodeal trophallaxis can be considered two sides of the same coin. From the host point of view proctodeal trophallaxis marks the origination of parental care by provisioning neonates with nourishment, metabolites and beneficial microbiota. From the flagellate point of view, proctodeal trophallaxis was a shift from horizontal to vertical transmission, pushing them from the parasitic to the mutualistic end of the symbiotic spectrum, arguably making this host behavioral change the most critical juncture in the evolutionary trajectory of the termite lineage.

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Gut bacteria mediate aggregation in the German cockroach

Cited by 159 publications

References 58 publications

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

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

Common bed bugs can biosynthesize pheromone components from amino acid precursors in human blood

Origin of Mutualism Between Termites and Flagellated Gut Protists: Transition From Horizontal to Vertical Transmission

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