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1 Lehrstuhl für Mikrobielle Ökologie, Fachbereich Biologie, Universität Konstanz, Fach M 654, 78457 Konstanz, Germany
2 Lehrstuhl für Mikrobiologie, Technische Universität München, Am Hochanger 4, 85350 Freising, Germany
Correspondence
Andreas Brune
Andreas.Brune{at}uni-konstanz.de
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The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of strains TmAO3T and TmAM3 are AJ506191 and AJ506192, respectively.
Present address: Botany Department, Jomo Kenyatta University of Agriculture and Technology, PO Box 62000, Nairobi, Kenya. 
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. In the following years, the presence of homoacetogenic activity has been demonstrated for a large number of termite species from all major feeding guilds, including representatives of wood-feeding, fungus-cultivating and soil-feeding termites (Brauman et al., 1992). Although reductive acetogenesis was always out-competed as a hydrogen sink by methanogenesis in gut homogenates of soil-feeding termites (Brauman et al., 1992), microinjection of H14CO3- into intact hindguts of soil-feeding Cubitermes spp. has identified a high potential for reductive acetogenesis (Tholen & Brune, 1999), indicating that the contribution of reductive acetogenesis to overall electron flow in the guts of soil-feeding termites may be larger than expected.
In order to define the metabolic potential of termite gut homoacetogens and to identify specific adaptations to the gut environment, it is necessary to study these bacteria in pure culture (Brune et al., 2000). However, only five strains of homoacetogenic bacterium have so far been isolated from termite guts, four of them from wood-feeding species. They comprise Sporomusa termitida and Acetonema longum from Nasutitermes nigriceps and Pterotermes occidentis (Breznak et al., 1988; Kane & Breznak, 1991) and two spirochaetal isolates, strains ZAS-1 and ZAS-2, from Zootermopsis angusticollis (Leadbetter et al., 1999). Only one homoacetogenic bacterium, Clostridium mayombei (Kane et al., 1991), has been obtained from a soil-feeding termite (Cubitermes speciosus). Nevertheless, each of these isolates was a member of a novel genus or species affiliated with a different phylogenetic group and it is reasonable to assume that they represent only a negligible fraction of the diversity of homoacetogens that colonize the guts of more than 2600 known species of termite (Kambhampati & Eggleton, 2000).
Clearly, more isolates are needed to understand the physiological role and ecological significance of homoacetogenic bacteria in termite guts. In this study, we describe the isolation and characterization of a novel homoacetogenic bacterium from the gut of the soil-feeding termite Thoracotermes macrothorax. Further physiological characterization of this strain, which is the subject of a separate study (Boga & Brune, 2003), led to the surprising discovery of high oxygen-reducing capacity in this and other homoacetogenic bacteria isolated from termite guts.
Isolation and morphological characterization
Gut homogenates were prepared from different gut sections of the termite Thoracotermes macrothorax Sjöstedt (Tholen & Brune, 1999) and diluted serially in anoxic, bicarbonate-buffered mineral medium (AM-5) supplemented with yeast extract and Casamino acids (each 0·1 %, w/v) (Boga & Brune, 2003). Enrichment cultures with lactate (8 mM) as an additional substrate and DTT (1 mM) as a reducing agent were incubated in an H2/CO2 atmosphere (80 : 20, v/v; 150 kPa). The highest dilutions where net acetate production indicated the presence of reductive acetogenesis were transferred into fresh medium. Subsequent agar dilution series (Pfennig & Trüper, 1981), conducted in the same medium but incubated in an N2/CO2 atmosphere, yielded mostly light-brown, lentil-shaped colonies from which several pure cultures were obtained.
Phase-contrast microscopy revealed morphologically indistinguishable, curved rods with slightly tapered ends, which resembled the shape of a banana. Strain TmAM3, which was derived from a homogenate of midgut and mixed segment, and strain TmAO3T, which stemmed from a homogenate that comprised the third and fourth proctodeal segment, were selected for further characterization. In each case, the dilution steps indicated an original population of approximately 103–104 cells per gut section.
Both strains stained Gram-positive but reacted Gram-negative in the KOH test (Gregersen, 1978); Bacillus megaterium (DSM 32T) and Escherichia coli (DSM 498) were used as controls. Cells of strain TmAO3T were 3–7 µm long and 0·6–0·7 µm wide and occurred singly or in pairs (Fig. 1a). In the stationary growth-phase, they formed terminal endospores in club-shaped sporangia that tended to aggregate in a characteristic manner (Fig. 1b). Older cultures sporulated completely and remained viable when pasteurized (80 °C, 10 min). Cells were motile by means of one or more lateral flagella (Figs 1c and d). Identical results were obtained with strain TmAM3.
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). Aromatic acids were quantified by reversed-phase HPLC as described previously (Brune & Schink, 1990).
Both strains required an oxygen-free, reduced medium for growth. They grew best in medium reduced with DTT (1 mM) or cysteine (2 mM). Good growth was also obtained when a palladium catalyst was added to reduce medium incubated in an H2/CO2 atmosphere (Tholen et al., 1997). The strains grew homoacetogenically on H2/CO2 or L-lactate but required small amounts (0·1 %, w/v) of yeast extract or Casamino acids, which were fermented to acetate and traces of propionate. As the results of all initial growth tests were identical for both isolates, only strain TmAO3T was characterized in more detail.
On basal medium with lactate, cells grew at pH 6·2–8·2 [pH adjusted by adding sterile Na2CO3 (1 M) or HCl (1 M)] and at 19–35 °C, but not at 4 or 40 °C. Highest growth yields were obtained at 30 °C and pH 7. Under these conditions, cultures reached similar densities on H2/CO2 (80 : 20; 150 kPa) or lactate (8·1 mM) (Fig. 2), but the respective growth yields differed considerably [2·5 and 6·0 g dry wt (mol acetate)-1, corrected for background growth and acetate production on basal medium]. Doubling times of cultures growing on H2/CO2 or lactate were 8·9 and 4·4 h, respectively. In cultures growing on H2/CO2, growth was exponential only at lower cell densities. Most likely, mass transfer of H2 from the gas phase into the liquid medium became limiting as cell density increased.
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), i.e. all reducing equivalents from substrate oxidation to acetate were apparently used for further (reductive) acetogenesis from CO2.
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). Strain TmAO3T also grew by demethylation of vanillate, syringate and 3,4,5-trimethoxybenzoate (each 2 mM), forming acetate and the corresponding phenolates (protocatechuate or gallate) as demethylation products. No growth occurred with glucose, fructose, lactose, cellobiose, trehalose or ethylene glycol (5 or 10 mM each) or with glycerol, oxalate, glyoxylate, aspartate or glutamate (10 or 20 mM each). Sulfate and nitrate (10 mM each) were not reduced (this was tested with lactate as electron donor).
Cytochrome content
Cultures were centrifuged at 10 000 g for 30 min and cells were washed and then resuspended in anoxic buffer. Cell extracts were prepared by repeatedly passing the cell suspension through a French pressure cell at 138 MPa. Crude extract was centrifuged again (30 000 g, 20 min) and the supernatant (cell-free extract) was fractionated into a membrane fraction and a soluble fraction by ultracentrifugation (126 000 g, 1 h). Fractions were assayed for the presence of cytochromes by recording difference spectra of N2S2O4-reduced minus air-oxidized samples, as described previously (Breznak et al., 1988). All procedures were carried out in potassium phosphate buffer (0·1 M, pH 7).
Redox difference spectra of cell extracts from lactate-grown (Fig. 3) and hydrogen-grown (not shown) cells of strain TmAO3T showed absorption maxima at 562, 545 and 432 nm, which are characteristic of b-type cytochrome(s) (Dickerson & Timkovich, 1975). Absence of other absorption maxima and the fact that maxima were found only in the spectra of the membrane fraction after ultracentrifugation indicated that a- or c-type cytochromes were not present.
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). The 16S rRNA gene sequences (homologous to E. coli positions 8–1542) of the isolates were fitted into an alignment of about 40 000 homologous full or partial primary structures that are available in public databases (Ludwig, 1995) by using the automated tools of the ARB software package (Ludwig & Strunk, 1996). Distance-matrix, maximum-parsimony and maximum-likelihood methods were applied for tree construction, as implemented in the ARB software package. Different datasets, which varied with respect to the selection of outgroup reference organisms as well as alignment positions, were analysed.
The almost-complete 16S rRNA gene sequences obtained for strains TmAO3T and TmAM3 were nearly identical (>99·5 % sequence similarity). Comparative sequence analysis revealed that both strains were phylogenetically most closely related to members of the genus Sporomusa (Fig. 4), which belongs to a subgroup of Gram-positive bacteria with a low DNA G+C content that is characterized by organisms with a Gram-negative cell wall (Willems & Collins, 1995). All phylogenetic analyses placed the sequences of strains TmAO3T and TmAM3 at the base of the Sporomusa species cluster; sequence similarity to other members of the genus Sporomusa ranged from 94 to 97 %. Highest values were obtained with Sporomusa sphaeroides (96·8 %) and Sporomusa sp. strain DR5 (97·0 %), which was isolated from anoxic bulk soil of flooded rice microcosms (Rosencrantz et al., 1999). Sequence similarity to representatives of other genera in the subgroup was <91·6 %.
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). Also, the demethylation of O-methyl ethers and subsequent fermentation of the methyl groups to acetate and the utilization of other C1 compounds such as formate and methanol are typical of many homoacetogens (see reviews by Diekert, 1992; Drake et al., 1994; Schink, 1994).
16S rRNA gene sequence analysis revealed that strains TmAO3T and TmAM3 are most closely related to members of the genus Sporomusa. Their phenotypic characteristics are also typical of members of this genus (Möller et al., 1984): cells are curved, banana-shaped rods, form heat-resistant endospores, are motile by one or more lateral flagella, possess b-type cytochromes and form acetate as the major fermentation product.
In its substrate utilization spectrum, strain TmAO3T most closely resembles S. termitida, a homoacetogenic isolate from a wood-feeding termite (Breznak et al., 1988), which was included in this study as a reference strain. Both strains can be clearly differentiated from other members of the genus Sporomusa by their inability to grow on fructose and glycerol and their ability to grow on mannitol, citrate and succinate (Table 2). However, the strains differ significantly in their 16S rRNA gene sequence (94 % similarity) and the ability to ferment dicarboxylic acids. Strain TmAO3T grows on L-malate and fumarate, whereas cells of S. termitida do not grow on these substrates (Table 2). Cells of strain TmAO3T are also curved more strongly and, in contrast to S. termitida, are not sensitive to reducing agents such as DTT and cysteine (Breznak et al., 1988; this study).
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; Drake et al., 1997), strain TmAO3T is metabolically quite versatile. It ferments a large number of organic substrates homoacetogenically, utilizing reductive acetogenesis from CO2 as an acceptor for the electrons released during substrate oxidation to acetate. The inability to ferment glucose or other sugars is unusual but encountered frequently among Sporomusa species (Table 2). Also, fermentation of dicarboxylic acids, e.g. fumarate and L-malate, is not a common trait among homoacetogens, but again, it is not uncommon in the genus Sporomusa (Table 2). It has been suggested that b-type cytochromes, which are present in many Sporomusa species (including strain TmAO3T), are involved in fumarate reduction (Diekert, 1992; Diekert & Wohlfarth, 1994). However, b-type cytochromes are also present in species that do not grow on dicarboxylic acids (S. termitida, Sporomusa ovata and S. sphaeroides) and there is evidence for S. sphaeroides that b-type cytochromes are also involved in the oxidation of methyl groups (Kamlage & Blaut, 1993).
Molecular hydrogen is a typical product that is formed by fermentative degradation of organic compounds (Schink, 1997) and hydrogen-consuming processes, such as reductive acetogenesis and methanogenesis, seem to be important electron sinks in the hindguts of all termites studied so far (Brauman et al., 1992; Schmitt-Wagner & Brune, 1999; Tholen & Brune, 1999). In soil-feeding Termitinae, methanogenesis seems to dominate over reductive acetogenesis as a hydrogen sink, possibly due to the lower affinity of homoacetogens for H2 (Breznak, 1994). Nevertheless, the presence of high potential rates of reductive acetogenesis in soil-feeding termites indicates that they are able to coexist with other hydrogenotrophic populations (Tholen & Brune, 1999).
It is possible that the metabolic versatility of homoacetogenic bacteria allows them to maintain an active metabolism during phases of low H2 partial pressure in the gut (Tholen & Brune, 1999). Hindgut fluid of soil-feeding termites contains considerable concentrations of potential substrates for homoacetogens, e.g. lactate and ethanol (E. Miambi, H. I. Boga, A. Tholen & A. Brune, unpublished data), and probably also methoxylated aromatic compounds that are derived from lignins or humic acids. Recent findings indicate that peptides and amino acids may also be important substrates for the gut microbiota of soil-feeding termites (Ji et al., 2000). Mixotrophy, i.e. the ability of homoacetogens to use H2 and organic substrates simultaneously, as observed for S. termitida (Breznak & Blum, 1991), would add to their competitiveness (Breznak, 1994).
Strain TmAO3T was isolated from a dilution step that indicated a population of approximately 103–104 cells per gut section, which is in good agreement with the estimated total number of homoacetogens growing in serial dilutions of gut homogenates of Thoracotermes macrothorax (E. Miambi, H. I. Boga, A. Tholen & A. Brune, unpublished data). Nevertheless, the large discrepancy between viable counts and total cell counts, together with the high potential rates of reductive acetogenesis in the guts of soil-feeding termites, indicate a strong cultivation bias against homoacetogens (Tholen & Brune, 1999).
Oxygen reduction
Drake and coworkers were the first to document tolerance and metabolic response to the presence of oxygen for a number of homoacetogens, including Sporomusa silvacetica (Küsel et al., 2001; Karnholz et al., 2002). In an independent study, we have shown that strain TmAO3T and other strains of homoacetogen isolated from termite guts consume oxygen at high rates (Boga & Brune, 2003).
Strain TmAO3T has by far the highest capacity for hydrogen-dependent oxygen reduction [826 nmol min-1 (mg protein)-1] of all homoacetogens tested (Boga & Brune, 2003); it is surpassed only by that reported for several Desulfovibrio species isolated from termite guts (Kuhnigk et al., 1996; Cypionka, 2000). The activity is cyanide-sensitive, which indicates that cytochromes might participate in electron transport to oxygen. Strain TmAO3T also possesses high catalase activity, whereas it is superoxide dismutase-negative in both the xanthine/xanthine oxidase assay and the nitro blue tetrazolium salt reduction assay (Boga & Brune, 2003).
Owing to its large capacity for hydrogen-dependent oxygen reduction and its exceptional tolerance to a temporary exposure to oxygen, strain TmAO3T is able to initiate growth in non-reduced basal medium that contains up to 1·5 kPa of oxygen in the headspace (Boga & Brune, 2003). However, closer investigation revealed that growth commences only after the cells have rendered the medium anoxic and that reductive acetogenesis from CO2 is severely compromised if even traces of oxygen are present in the medium (Boga & Brune, 2003).
It has been proposed that the ability of obligate anaerobes to scavenge oxygen, together with their apparent tolerance of toxic oxygen reduction products, would not only enable them to survive a temporary exposure to oxygen but would also allow them to actively re-establish favourable conditions for growth (Boga & Brune, 2003). As the termite gut habitat is characterized by a large influx of oxygen via the epithelium (Brune, 1998; Brune et al., 2000), it is possible that strain TmAO3T contributes to oxygen consumption within the micro-oxic periphery of the gut.
Based on phylogenetic, morphological and physiological differences, strain TmAO3T is proposed as a novel member of the genus Sporomusa, with the name Sporomusa aerivorans sp. nov.
Description of Sporomusa aerivorans sp. nov.
Sporomusa aerivorans [ae.ri.vo'rans. L. n. aer air; L. pres. part. vorans digesting, devouring; N.L. pres. part. aerivorans devouring air (oxygen), referring to the high capacity of the organism to reduce oxygen].
Curved rods, 1·3–7·0 µm long and 0·6–0·7 µm wide. Motile by one or more lateral flagella. Stain Gram-positive but react Gram-negative in the KOH test. Catalase-positive but superoxide dismutase-negative. Terminal, heat-resistant endospores in club-shaped sporangia are formed. Oxygen-sensitive; does not grow in air. Resting cells reduce oxygen in the presence of hydrogen or by endogenous reductant; therefore, they can initiate growth in non-reduced medium under micro-oxic conditions. Chemo-organotrophic fermentative metabolism. Nitrate and sulfate are not used as external electron acceptors. Grows lithotrophically by reductive acetogenesis on H2 and CO2 in the presence of yeast extract or Casamino acids. Homoacetogenic; ferments L-lactate, pyruvate, citrate, L-alanine, D-mannitol, ethanol, formate and methanol to acetate as sole product. Fumarate, L-malate and oxaloacetate are fermented to propionate and acetate. Decarboxylates succinate and malonate to propionate or acetate, respectively. The O-methyl groups of syringate, vanillate and 3,4,5-trimethoxybenzoate are fermented to acetate. Does not grow on hexoses. Yeast extract or Casamino acids are required for growth and are fermented mainly to acetate. Possesses membrane-bound b-type cytochrome(s). Temperature range for growth is 19–35 °C, optimum 30 °C. No growth at 4 or 45 °C. pH range for growth is 6·2–8·2, optimum pH 7.
Type strain: TmAO3T (=DSM 13326T=ATCC BAA-625T). Habitat: intestinal tract of the termite Thoracotermes macrothorax.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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) or H2/CO2 (80 : 20; 150 kPa) (
) in basal medium that contained yeast extract and Casamino acids (each 0·1 %, w/v). Background growth on basal medium alone (
). Values are means of two cultures.
