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Appl. Environ. Microbiol., Jul 1995, 2681-2687, Vol 61, No. 7
A Brune, D Emerson and JA Breznak
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.
Copyright © 1995, American Society for Microbiology
The Termite Gut Microflora as an Oxygen Sink: Microelectrode Determination of Oxygen and pH Gradients in Guts of Lower and Higher Termites
Department of Microbiology and Center for Microbial Ecology, Michigan State University, East Lansing, Michigan 48824-1101
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