Communities of microbes that inhabit the changing hindgut landscape of a subsocial beetle

Nardi, James B.; Bee, Charles Mark; Miller, Lou Ann; Nguyen, Nhu; Suh, Sung Oui; Blackwell, Meredith

doi:10.1016/j.asd.2005.06.003

Cited by 58 publications

(45 citation statements)

References 22 publications

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“…In this study, we provide the first insight into microbial community assembly, one aspect of its function (N-fixation) and physiological gradients (O 2 , pH) that may regulate microbial composition and activity in this beetle's digestive tract. We hypothesized that the morphological and physiological differences observed among gut regions (Nardi et al, 2006) Figure 6 (a) Average probe-set positive fraction for methanogenic groups at each gut region (n ¼ 4). (b) Average of the normalized probeset intensity for methanogenic groups at the AHG (n ¼ 4).…”

Section: Discussionmentioning

confidence: 99%

“…The continuous movement of the electrode tip through the beetle gut until it reached the opposite side showed profiles of O 2 that mirrored those obtained when entering the gut. By measuring the gut wall thickness of the AHG and PHG from the images reported by Nardi et al (2006) and according to the O 2 profiles determined in this paper, all gut regions are characterized by a rapid transition from microaerophilic to anaerobic conditions in the lumen. The extent of oxygen availability varied by gut region, being 4300 mm into the lumen in the FG and MG when considering gut wall thickness o100 mm compared with approximately 50 and 280 mm for the AHG and PHG, respectively, where gut wall thicknesses were 200 and 110 mm.…”

Section: Oxygen Profilesmentioning

confidence: 99%

“…Pichia stipitis), that has the ability to ferment xylose, a significant component of hemicellulose (Shi et al, 2010). In a detailed study of O. disjunctus gut morphology and gut inhabitants, Nardi et al (2006) divided each gut into four morphologically distinct regions where the gut biota appears to be differentiated as noted previously for fungus-like organisms known as trichomycetes (Lichtwardt et al, 1999).…”

Section: Introductionmentioning

confidence: 99%

“…reviewed in Brune and Ohkuma, (2011)). The gut microbiome of wood-feeding beetles likely overcomes similar N constraints, and certain beetles have received recent attention regarding their digestive tract morphology and culturable fungal communities (Slaytor, 1992;Suh et al, 2003;Nardi et al, 2006;Klass et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

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Compartmentalized microbial composition, oxygen gradients and nitrogen fixation in the gut ofOdontotaenius disjunctus

et al. 2013

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Coarse woody debris is an important biomass pool in forest ecosystems that numerous groups of insects have evolved to take advantage of. These insects are ecologically important and represent useful natural analogs for biomass to biofuel conversion. Using a range of molecular approaches combined with microelectrode measurements of oxygen, we have characterized the gut microbiome and physiology of Odontotaenius disjunctus, a wood-feeding beetle native to the eastern United States. We hypothesized that morphological and physiological differences among gut regions would correspond to distinct microbial populations and activities. In fact, significantly different communities were found in the foregut (FG), midgut (MG)/posterior hindgut (PHG) and anterior hindgut (AHG), with Actinobacteria and Rhizobiales being more abundant toward the FG and PHG. Conversely, fermentative bacteria such as Bacteroidetes and Clostridia were more abundant in the AHG, and also the sole region where methanogenic Archaea were detected. Although each gut region possessed an anaerobic core, micron-scale profiling identified radial gradients in oxygen concentration in all regions. Nitrogen fixation was confirmed by 15 N 2 incorporation, and nitrogenase gene (nifH) expression was greatest in the AHG. Phylogenetic analysis of nifH identified the most abundant transcript as related to Ni-Fe nitrogenase of a Bacteroidetes species, Paludibacter propionicigenes. Overall, we demonstrate not only a compartmentalized microbiome in this beetle digestive tract but also sharp oxygen gradients that may permit aerobic and anaerobic metabolism to occur within the same regions in close proximity. We provide evidence for the microbial fixation of N 2 that is important for this beetle to subsist on woody biomass.

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Section: Discussionmentioning

confidence: 99%

Section: Oxygen Profilesmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Compartmentalized microbial composition, oxygen gradients and nitrogen fixation in the gut ofOdontotaenius disjunctus

et al. 2013

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“…Gut microbes also play a role in invertebrate biology (Dillon and Dillon, 2003) and digestive process [Brune, 2011 [Lundgren, 2010, and recently the composition of microbe gut populations has been described in a variety of insect species, including bees (Jeyaprakash et al, 2003;Mohr and Tebbe, 2006), beetles (Egert et al, 2005;Lehman et al, 2009;Nardi et al, 2006;Zhang and Jackson, 2008), flies (Cox and Gilmore, 2007;Ren et al, 2007;Ryu et al, 2008;Shin et al, 2011;Wong et al, 2011), lepidopterans (Pauchet et al, 2010;Xiang et al, 2006) and termites (Hongoh et al, 2003). In Drosophila, the microbiome regulates host metabolic homeostatic and developmental programs by modulating the insulin/insulin-like growth factor (Shin et al, 2011).…”

Section: Microbiota: a Key Component Of Nutritional Immunologymentioning

confidence: 99%

Integrating nutrition and immunology: A new frontier

Ponton

Wilson

Holmes

et al. 2013

Journal of Insect Physiology

127

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Elongated hindguts in desert‐living dung beetles (Scarabaeidae: Scarabaeinae) feeding on dry dung pellets or plant litter

Holter

Scholtz

2013

Journal of Morphology

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Most adult dung beetles (Scarabaeidae: Scarabaeinae) feed on fresh, wet dung of larger herbivorous or omnivorous mammals. As indigestible plant fragments are filtered out before ingestion, the food is presumed easily digestible. However, members of the desert-living scarabaeine genus Pachysoma (probably evolved from an ancestor closely related to the wet-dung feeding genus Scarabaeus) select dry dung pellets and/or plant litter. Thus they ingest a much higher proportion of refractory plant material which, interestingly, seems to be digested rather efficiently. This study investigates morphological modifications of the gut for this digestion in adults of eight Pachysoma species, both pellet and litter feeders. To ascertain hypothesized ancestral conditions, four fresh-dung feeding Scarabaeus species were also examined. The latter Presumably, plant fragments in the food are digested, at least partly, in the hindgut. If so, the morphological adaptation is unusual: simple elongation rather than expansion of part of the hindgut, as found in several other plant-or detritus-feeding scarabs.

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Communities of microbes that inhabit the changing hindgut landscape of a subsocial beetle

Cited by 58 publications

References 22 publications

Compartmentalized microbial composition, oxygen gradients and nitrogen fixation in the gut ofOdontotaenius disjunctus

Compartmentalized microbial composition, oxygen gradients and nitrogen fixation in the gut ofOdontotaenius disjunctus

Integrating nutrition and immunology: A new frontier

Elongated hindguts in desert‐living dung beetles (Scarabaeidae: Scarabaeinae) feeding on dry dung pellets or plant litter

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