Deletion Analysis of the Escherichia coli Taurine and Alkanesulfonate Transport Systems

Abstract

The Escherichia coli tauABCD and ssuEADCB gene clusters are required for the utilization of taurine and alkanesulfonates as sulfur sources and are expressed only under conditions of sulfate or cysteine starvation. tauD and ssuD encode an ␣-ketoglutarate-dependent taurine dioxygenase and a reduced flavin mononucleotidedependent alkanesulfonate monooxygenase, respectively. These enzymes are responsible for the desulfonation of taurine and alkanesulfonates. The amino acid sequences of SsuABC and TauABC exhibit similarity to those of components of the ATP-binding cassette transporter superfamily, suggesting that two uptake systems for alkanesulfonates are present in E. coli. Chromosomally located in-frame deletions of the tauABC and ssuABC genes were constructed in E. coli strain EC1250, and the growth properties of the mutants were studied to investigate the requirement for the TauABC and SsuABC proteins for growth on alkanesulfonates as sulfur sources. Complementation analysis of in-frame deletion mutants confirmed that the growth phenotypes obtained were the result of the in-frame deletions constructed. The range of substrates transported by these two uptake systems was largely reflected in the substrate specificities of the TauD and SsuD desulfonation systems. However, certain known substrates of TauD were transported exclusively by the SsuABC system. Mutants in which only formation of hybrid transporters was possible were unable to grow with sulfonates, indicating that the individual components of the two transport systems were not functionally exchangeable. The TauABCD and SsuEADCB systems involved in alkanesulfonate uptake and desulfonation thus are complementary to each other at the levels of both transport and desulfonation.In Escherichia coli, sulfate starvation causes increased synthesis of several proteins involved in scavenging sulfur from alternative sulfur sources (15). Recently, two sets of genes whose expression is derepressed in the absence of sulfate or cysteine were identified. The tauABCD gene cluster, located at 8.5 min on the E. coli chromosome, encodes a sulfonate-sulfur utilization system that is specifically involved in the utilization of taurine (2-aminoethanesulfonic acid) as a source of sulfur. Disruption of tauB, tauC, or tauD resulted in the loss of the ability to utilize taurine as a source of sulfur but did not affect the utilization of a range of other aliphatic sulfonates (21). The TauD protein is an ␣-ketoglutarate-dependent taurine dioxygenase (3), and the TauABC proteins exhibit similarity to ATP-binding cassette (ABC)-type transport systems (21). A second set of genes, the ssuEADCB gene cluster, located at 21.4 min on the chromosome, enables E. coli to utilize aliphatic sulfonates other than taurine as a source of sulfur. Deletion of ssuEADCB caused an inability to utilize alkanesulfonates but did not affect the utilization of taurine (24). SsuD is a monooxygenase that catalyzes the desulfonation of a wide range of sulfonated substrates other than taurine, including C 2 to C 10...

Unravelling the complete genome sequence of Advenella mimigardefordensis strain DPN7T and novel insights in the catabolism of the xenobiotic polythioester precursor 3,3′-dithiodipropionate

“…The active inter-conversion of organic and inorganic sulfur forms in soil is due to microbial activities, and a plant-growth-promoting effect was demonstrated for desulfonating bacterial strains (Kertesz & Mirleau, 2004;Schmalenberger & Kertesz, 2007;Schmalenberger et al, 2008). The ssu genes are known to be responsible for uptake and degradation of aliphatic sulfonates other than taurine (Eichhorn et al, 2000); accordingly, nine putative ssuABC clusters, which code for ABC-type aliphatic sulfonate transport systems, were identified in the genome of A. mimigardefordensis strain DPN7 T (Table S3). Interestingly, the ssuCBA genes with the locus tag MIM_c03970-MIM_c03990 are encircled by two tauD (MIM_c03960, MIM_c04000).…”

“…Taurine is a non-proteinogenic amino acid, and occurs as a major organic solute in all vertebrates and in a wide range of marine invertebrates. In E. coli, the use of taurine as a sulfur source was attributed to the tauABCD gene cluster that encodes a specialized sulfonate-sulfur utilization (ssu) system, which is in most cases exclusively involved in utilization of this substrate (van der Ploeg et al, 1996;Eichhorn et al, 2000;Cook et al, 2006). A. mimigardefordensis strain DPN7 T was able to grow with taurine as the sole source of carbon and sulfur (Wübbeler et al, 2008).…”

“…S1H) is flanked by all the three genes in the genome that encode alkanesulfonate monooxygenases SsuD (MIM_c01490, MIM_c01540, MIM_c01550) and another ssuACB cluster (MIM_c01580-MIM_c01560). SsuD is able to desulfonate a wide range of aliphatic, but not aromatic sulfonates, with the above-mentioned exception of taurine (Eichhorn et al, 2000). To perform this desulfonation reaction, the two-component SsuD needs FMNH 2 as a substrate, which is provided by the associated FMN reductase SsuE (MIM_c01500).…”

Inducible transcription of genes involved in taurine uptake and dissimilation by Silicibacter pomeroyi DSS-3T

“…It involved an ATP binding-cassette transporter (TauABC) [TC 3.A.1.17.1], a taurine:pyruvate aminotransferase (Tpa) [EC 2.6.1.77], Xsc and phosphate acetyltransferase (Pta) [EC 2.3.1.8] (Moran et al 2004). The function of putative TauABC, orthologs of the Eschericha coli TauABC that was characterized in sulfur assimilation (Eichhorn et al 2000), has never been tested in a dissimilative pathway, and TauA shares only 23% identity with the characterized protein from E. coli. The putative Tpa shares 59 and 33% identity with the established orthologs in Bilophila wadsworthia RZATAU and Rhodococcus opacus ISO-5, respectively (Laue and Cook 2000a;Denger et al 2004).…”

Genome-enabled analysis of the utilization of taurine as sole source of carbon or of nitrogen by Rhodobacter sphaeroides 2.4.1

“…The hypothetical ABC transporter ('NsbABC'; Fig. 1b, Table 3) encoded upstream of this transaminase is a member of a large group of uncharacterized ABC transporters closely related to TC 3.A.1.12/16/17.-which are unfortunately termed TauABC, identical to the TauABC transporters involved in taurine metabolism (TC 3.A.1.17.1) (Eichhorn et al, 2000;Gorzynska et al, 2006). TauA and NsbA share <20 % sequence identity.…”