Multipartite interactions in firebug guts

Red firebugs and African cotton stainers (Pyrrhocoris apterus and Dysdercus fasciatus, Hemiptera: Pyrrhocoridae) harbor a community of Actinobacteria, Firmicutes, and Proteobacteria in the anoxic M3 region of their mid-gut. By targeted manipulation of the microbial community, we were able to demonstrate that the actinobacterial symbionts play an important role for the hosts’ fitness by supplementing B vitamins that are limiting in the bugs’ natural diet of Malvales plant seeds. Concordantly, aposymbiotic (= symbiont-free) bugs show slower growth rates, increased mortality, and lower reproductive success than symbiont-containing bugs. The symbionts are transmitted vertically via egg-smearing, but horizontal transmission can also occur by the uptake of symbionts from the feces of conspecific individuals. A broad survey of microbial communities associated with about 20 different Pyrrhocoridae and closely related bug species revealed the evolutionary origin of the symbiosis with vitamin-supplementing Actinobacteria in the late Cretaceous, coinciding with the evolution of their host plant order Malvales.

We are currently investigating the molecular basis of host-symbiont interactions in the firebug gut. Due to the localization of the symbionts and the composition of the microbial community, firebugs can serve as a model system for many organisms, including vertebrates. Specifically, we are interested in the host’s immune effectors involved in maintaining the specific microbial community, as well as the effect of both host and symbionts on infection with the specialized trypanosomatid parasite Leptomonas pyrrhocoris. Furthermore, we are assessing the potential of the bacterial symbionts for detoxifying noxious secondary metabolites of the host plants and the implications of this for the early evolution of the symbiosis.

Martin KaltenpothEugen Bauer, Thomas Ogao Onchuru, Adam Martinez

Selected publications:

Onchuru, T. O. & Kaltenpoth, M. (2019) Established cotton stainer gut bacterial mutualists evade regulation by host antimicrobial peptides. Applied and Environmental Microbiology. DOI: 10.1128/AEM.00738-19. 

Onchuru, T., Martinez, A., Kaltenpoth, M. (2018) The cotton stainer’s gut microbiota suppresses infection of a co-transmitted trypanosomatid parasite, Molecular Ecology, 27 (16): 3408-3419.

Salem, H., Onchuru, T.O., Bauer, E. & Kaltenpoth, M. (2015) Symbiont transmission entails the risk of parasite infection. Biology Letters.

Sudakaran, S., Retz, F., Kikuchi, Y., Kost, C. & Kaltenpoth, M. (2015) Evolutionary transition in symbiotic syndromes enabled diversification of phytophagous insects on an imbalanced diet. The ISME Journal.

Kaltenpoth, M. (2014) Vitamin-produzierende Symbionten in Feuerwanzen. BIOspektrum 02.14: 144-147.

Bauer, E., Salem, H., Marz, M., Vogel, H. & Kaltenpoth, M. (2014) Transcriptomic immune response of the cotton stainer Dysdercus fasciatus to experimental elimination of vitamin-supplementing intestinal symbionts. PLoS ONE 9 (12): e114865.

Salem, H., Bauer, E., Strauss, A.S., Vogel, H., Marz, M. & Kaltenpoth, M. (2014) Vitamin supplementation by gut symbionts ensures metabolic homeostasis in an insect host. Proceedings of the Royal Society B-Biological Sciences 281: 20141838.

Salem, H., Kreutzer, E., Sudakaran, S. & Kaltenpoth, M. (2013) Actinobacteria as essential symbionts in firebugs and cotton stainers (Hemiptera, Pyrrhocoridae). Environmental Microbiology 15 (7): 1956-1968.

Sudakaran, S., Salem, H., Kost, C. & Kaltenpoth, M. (2012) Geographic and ecological stability of the symbiotic mid-gut microbiota in European firebugs, Pyrrhocoris apterus (Hemiptera; Pyrrhocoridae). Molecular Ecology 21: 6134-6151.

Kaltenpoth, M., Winter, S. & Kleinhammer, A. (2009) Localization and transmission route of Coriobacterium glomerans, the endosymbiont of pyrrhocorid bugs. FEMS Microbiology Ecology 69 (3): 373-383.