Chemolithoautotrophy and mixotrophy in the thiophene-2-carboxylic acid-utilizing Xanthobacter tagetidis

Abstract

Xanthobacter tagetidis grew as a chemolithotrophic autotroph on thiosulfate and other inorganic sulfur compounds, as a heterotroph on thiophene-2-carboxylic acid, acetic acid and alpha-ketoglutaric acid, and as a mixotroph on thiosulfate in combination with thiophene-2-carboxylic acid and/or acetic acid. Autotrophic growth on one-carbon organosulfur compounds, and intermediates in their oxidation are also reported. Thiosulfate enhanced the growth yields in mixotrophic cultures, presumably by acting as a supplementary energy source, since ribulose bisphosphate carboxylase was only active in thiosulfate-grown cells and was not detected in mixotrophic cultures using thiosulfate with thiophene-2-carboxylic acid. Bacteria grown on thiophene-2-carboxylic acid also oxidized sulfide, thiosulfate and tetrathionate, indicating these as possible sulfur intermediates in thiophene-2-carboxylic acid degradation. Thiosulfate and tetrathionate were oxidized completely to sulfate and, consequently, did not accumulate as products of thiophene-2-carboxylic acid oxidation in growing cultures. Km and Vmax values for the oxidation of thiosulfate, tetrathionate or sulfide were 13 &mgr;M and 83 nmol O2 min-1 (mg dry wt.)-1, respectively; thiosulfate and tetrathionate became autoinhibitory at concentrations above 100 &mgr;M. The true growth yield (Ymax) on thiophene-2-carboxylic acid was estimated from chemostat cultures (at dilution rates of 0.034-0.094 h-1) to be 112.2 g mol-1, with a maintenance coefficient (m) of 0.3 mmol thiophene-2-carboxylic acid (g dry wt.)-1 h-1, and the maximum specific growth rate (&mgr;max) was 0.116 h-1. Growth in chemostat culture at a dilution rate of 0. 041 h-1 indicated growth yields [g dry wt. (mol substrate)-1] of 8.1 g (mol thiosulfate)-1, 60.9 g (mol thiophene-2-carboxylic acid)-1, and 17.5 g (mol acetic acid)-1, with additive yields for growth on mixtures of these substrates. At a dilution rate of 0.034 h-1, yields of 57.8 g (mol alpha-ketoglutaric acid)-1 and 60.7 g (mol thiophene-2-carboxylic acid)-1 indicated some additional energy conservation from oxidation of the thiophene-sulfur. SDS-PAGE of cell-free preparations indicated a polypeptide (Mr, 21.0 kDa) specific to growth on thiophene-2-carboxylic acid for which no function can yet be ascribed: no metabolism of thiophene-2-carboxylic acid by cell-free extracts was detected. It was shown that X. tagetidis exhibits a remarkable degree of metabolic versatility and is representative of facultatively methylotrophic and chemolithotrophic autotrophs that contribute significantly to the turnover of simple inorganic and organic sulfur compounds (including substituted thiophenes) in the natural environment.

Biochemistry and molecular biology of lithotrophic sulfur oxidation by taxonomically and ecologically diverse bacteria and archaea

“…Silicibacter pomeroyi ) (Kelly & Wood, 2000a; Moran et al , 2004; Anandham et al , 2007; Ghosh & Roy, 2007a). Under nutrient‐limited mixotrophic conditions Xanthobacter tagetidis (Padden et al , 1998) and Pseudaminobacter salicylatoxidans (Lahiri et al , 2006) show increases in growth and cellular yield over the autotrophic levels. Obligately chemolithotrophic unicellular sulfur‐oxidizing bacteria, on the other hand, belong to the Beta ‐ (e.g.…”

Physiological Versatility of the Extremely Thermoacidophilic Archaeon Metallosphaera sedula Supported by Transcriptomic Analysis of Heterotrophic, Autotrophic, and Mixotrophic Growth

“…Microbial mixotrophy has been defined as either the capacity to assimilate both organic and inorganic carbon sources simultaneously (18,20) or the utilization of an inorganic energy source in combination with an organic carbon source (1,16,21). Common to either definition is the idea that mixotrophy implicates a relationship between heterotrophy and autotrophy.…”

Metabolic adaptation and trophic strategies of soil bacteria—C1- metabolism and sulfur chemolithotrophy in Starkeya novella

“…(Stubner et al, 1998) and a recent description of a new Ancylobacter species, A. dichloromethanicus mentions growth as a facultative thiosulfate oxidizer as a trait of the species (Firsova et al, 2009). Similarly, Xanthobacter species including X. autotrophicus are known to be able to derive energy from thiosulfate oxidation, but the trait is not part of the species description, while the utilization of methanol as a growth substrate is recognized as a trait of the species (Padden et al, 1998; Stubner et al, 1998; Garrity et al, 2005). …”