Abstract
Clark-type oxygen microelectrodes and glass pH microelectrodes, each with a tip diameter of <=10 (mu)m, were used to obtain high-resolution profiles of oxygen concentrations and pH values in isolated termite guts. Radial oxygen profiles showed that oxygen penetrated into the peripheral hindgut contents up to about 150 to 200 (mu)m below the epithelial surface in both the lower termite Reticulitermes flavipes (Kollar) and the higher termite Nasutitermes lujae (Wasmann). Only the central portions (comprising less than 40% of the total volume) of the microbe-packed, enlarged hindgut compartments ("paunches") were completely anoxic, indicating that some members of the hindgut microbiota constitute a significant oxygen sink. From the slopes of the oxygen gradients, we estimated that the entire paunches (gut tissue plus resident microbiota) of R. flavipes and N. lujae accounted for 21 and 13%, respectively, of the respiratory activity of the intact animals. Axial oxygen profiles also confirmed that in general, only the paunches were anoxic in their centers, whereas midguts and posterior hindgut regions contained significant amounts of oxygen (up to about 50 and 30% air saturation, respectively). A remarkable exception to this was the posterior portion of an anterior segment (the P1 segment) of the hindgut of N. lujae, which was completely anoxic despite its small diameter ((apprx=)250 (mu)m). Axial pH profiles of the guts of Nasutitermes nigriceps (Haldeman) and Microcerotermes parvus (Haviland) revealed that there were extreme shifts as we moved posteriorly from the midgut proper (pH (apprx=)7) to the P1 segment of the hindgut (pH >10) and then to the P3 segment (paunch; pH (apprx=)7). The latter transition occurred at the short enteric valve (P2 segment) and within a distance of less than 500 (mu)m. In contrast, R. flavipes, which lacks a readily distinguishable P1 segment, did not possess a markedly alkaline region, and the pH around the midgut-hindgut junction was circumneutral. The oxic status of the peripheral hindgut lumen and its substantial oxygen consumption, together with previous reports of large numbers of aerobic and facultatively anaerobic bacteria in the hindgut microflora, challenge the notion that termite hindguts are a purely anoxic environment and, together with the steep axial pH gradients in higher termites, refine our concept of this tiny microbial habitat.
Full Text
The Full Text of this article is available as a PDF (610.1 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bignell D. E., Oskarsson H., Anderson J. M. Association of actinomycete-like bacteria with soil-feeding termites (termitidae, termitinae). Appl Environ Microbiol. 1979 Feb;37(2):339–342. doi: 10.1128/aem.37.2.339-342.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bignell D. E., Oskarsson H., Anderson J. M. Distribution and abundance of bacteria in the gut of a soil-feeding termite Procutiermes aburiensis (Termitidae, Termitinae). J Gen Microbiol. 1980 Apr;117(2):393–403. doi: 10.1099/00221287-117-2-393. [DOI] [PubMed] [Google Scholar]
- Breznak J. A. Intestinal microbiota of termites and other xylophagous insects. Annu Rev Microbiol. 1982;36:323–343. doi: 10.1146/annurev.mi.36.100182.001543. [DOI] [PubMed] [Google Scholar]
- Breznak J. A., Pankratz H. S. In situ morphology of the gut microbiota of wood-eating termites [Reticulitermes flavipes (Kollar) and Coptotermes formosanus Shiraki]. Appl Environ Microbiol. 1977 Feb;33(2):406–426. doi: 10.1128/aem.33.2.406-426.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brune A., Miambi E., Breznak J. A. Roles of oxygen and the intestinal microflora in the metabolism of lignin-derived phenylpropanoids and other monoaromatic compounds by termites. Appl Environ Microbiol. 1995 Jul;61(7):2688–2695. doi: 10.1128/aem.61.7.2688-2695.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Eutick M. L., O'Brien R. W., Slaytor M. Bacteria from the gut of Australian termites. Appl Environ Microbiol. 1978 May;35(5):823–828. doi: 10.1128/aem.35.5.823-828.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jensen K., Revsbech N. P., Nielsen L. P. Microscale distribution of nitrification activity in sediment determined with a shielded microsensor for nitrate. Appl Environ Microbiol. 1993 Oct;59(10):3287–3296. doi: 10.1128/aem.59.10.3287-3296.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Odelson D. A., Breznak J. A. Volatile Fatty Acid production by the hindgut microbiota of xylophagous termites. Appl Environ Microbiol. 1983 May;45(5):1602–1613. doi: 10.1128/aem.45.5.1602-1613.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schultz J. E., Breznak J. A. Heterotrophic bacteria present in hindguts of wood-eating termites [Reticulitermes flavipes (Kollar)]. Appl Environ Microbiol. 1978 May;35(5):930–936. doi: 10.1128/aem.35.5.930-936.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]