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, 78 (13), 4691-701

High-resolution Analysis of Gut Environment and Bacterial Microbiota Reveals Functional Compartmentation of the Gut in Wood-Feeding Higher Termites (Nasutitermes Spp.)

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High-resolution Analysis of Gut Environment and Bacterial Microbiota Reveals Functional Compartmentation of the Gut in Wood-Feeding Higher Termites (Nasutitermes Spp.)

Tim Köhler et al. Appl Environ Microbiol.

Abstract

Higher termites are characterized by a purely prokaryotic gut microbiota and an increased compartmentation of their intestinal tract. In soil-feeding species, each gut compartment has different physicochemical conditions and is colonized by a specific microbial community. Although considerable information has accumulated also for wood-feeding species of the genus Nasutitermes, including cellulase activities and metagenomic data, a comprehensive study linking physicochemical gut conditions with the structure of the microbial communities in the different gut compartments is lacking. In this study, we measured high-resolution profiles of H(2), O(2), pH, and redox potential in the gut of Nasutitermes corniger termites, determined the fermentation products accumulating in the individual gut compartments, and analyzed the bacterial communities in detail by pyrotag sequencing of the V3-V4 region of the 16S rRNA genes. The dilated hindgut paunch (P3 compartment) was the only anoxic gut region, showed the highest density of bacteria, and accumulated H(2) to high partial pressures (up to 12 kPa). Molecular hydrogen is apparently produced by a dense community of Spirochaetes and Fibrobacteres, which also dominate the gut of other Nasutitermes species. All other compartments, such as the alkaline P1 compartment (average pH, 10.0), showed high redox potentials and comprised small but distinct populations characteristic for each gut region. In the crop and the posterior hindgut compartments, the community was even more diverse than in the paunch. Similarities in the communities of the posterior hindgut and crop suggested that proctodeal trophallaxis or coprophagy also occurs in higher termites. The large sampling depths of pyrotag sequencing in combination with the determination of important physicochemical parameters allow cautious conclusions concerning the functions of particular bacterial lineages in the respective gut sections to be drawn.

Figures

Fig 1
Fig 1
Intestinal tract of Nasutitermes corniger. The gut includes the crop (C), midgut (M), mixed segment (ms), and several hindgut segments (P1 to P5); the asterisk marks the position of the P2 (enteric valve).
Fig 2
Fig 2
Axial profiles of oxygen (●) and hydrogen (○) partial pressure (A) and of redox potential (▲) and pH (▵) (B) along the gut of Nasutitermes corniger, measured at the gut center. Values are means ± standard errors obtained with 8 to 12 termites (except for the crop, which was lost in about half of the preparations). For definitions of the abbreviations of the gut compartments, see the legend to Fig. 1.
Fig 3
Fig 3
Radial profiles of oxygen (●) and hydrogen (○) partial pressure in the agarose-embedded anterior P3 compartment of Nasutitermes corniger relative to the agarose surface. The dotted lines indicate the positions of the proximal and distal gut wall. The profiles were selected as being typical among six similar sets obtained with different termites.
Fig 4
Fig 4
Relative abundance of major bacterial phyla in the different gut compartments of Nasutitermes corniger, based on pyrotag analysis of the V3-V4 region of the 16S rRNA genes. The area of the circles reflects the microbial cell counts in the respective gut sections (Table 1). For definitions of the abbreviations, see the legend to Fig. 1.
Fig 5
Fig 5
Relative abundance of the major bacterial taxa in the different gut sections of Nasutitermes corniger (for definitions of the abbreviations, see the legend to Fig. 1) and in the total hindguts of N. corniger and N. takasagoensis. Classification is shown down to the family level (for genus level, see Table S1 in the supplemental material). The heat map uses a logarithmic scale to increase the visibility of low-abundance groups. The remaining sequences were extremely diverse (111 to 157 families), but each represented less than 1% of the community in the respective compartment (see Table S1 in the supplemental material). The families represented in previously published clone libraries of N. takasagoensis (26) (total gut) and a Nasutitermes sp. (73) (P3 lumen) are shown for comparison (shading of circles indicates relative abundance).

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