Iron reduction in the metal-rich guts of wood-feeding termites

Termites play important roles in lignocellulose and humus turnover in diverse terrestrial ecosystems, and are significant sources of global atmospheric methane and carbon dioxide. All known termite species engage in obligate, complex nutritional symbioses with their gut microbes to carry out such processes. Several hundred microbial species, representing a broad phylogenetic and physiological diversity, are found within the well-bounded, microliterin-scale gut ecosystem of a given termite. However, most of these species have never been obtained in laboratory culture, and little can be said about their functional roles in the gut community or symbiosis. Herein, an unappreciated facet of the gut chemistry and microbiology of wood-feeding termites is revealed: the redox metabolism of iron. Gut fluids from field-collected termites contained millimolar amounts of ferrous iron and other heavy metals. When iron(III) hydroxides were amended to a filter paper diet of Zootermopsis nevadensis, a dampwood termite collected in the San Gabriel Mountains of Southern California, the specimens accumulated high levels of iron(II) in their guts. Additionally, iron was reduced at rapid initial rates in anoxic gut homogenates prepared from field-collected Z. nevadensis specimens. A Clostridium sp. and a Desulfovibrio sp. were isolated from dilution-to-extinction enrichments of Z. nevadensis gut contents and were found to reduce iron(III), as did the termite gut spirochete Treponema primitia. The iron in the guts of wood-feeding termites may influence the pathways of carbonand electron-flow, as well as microbial community composition in these tiny ecosystems of global importance. Received 28 September 2004; accepted 29 December 2004 Corresponding author: Jared R. Leadbetter. Tel.: (626) 395-4182; fax: (626) 395-2940; e-mail: [email protected]