The Adhesion-Associated sca Operon in Streptococcus gordonii Encodes an Inducible High-Affinity ABC Transporter for Mn ²⁺ Uptake

Abstract

ScaA lipoprotein in Streptococcus gordonii is a member of the LraI family of homologous polypeptides found among streptococci, pneumococci, and enterococci. It is the product of the third gene within the scaCBA operon encoding the components of an ATP-binding cassette (ABC) transporter system. Inactivation ofscaC (ATP-binding protein) or scaA(substrate-binding protein) genes resulted in both impaired growth of cells and >70% inhibition of 54Mn2+ uptake in media containing <0.5 μM Mn2+. In wild-type andscaC mutant cells, production of ScaA was induced at low concentrations of extracellular Mn2+ (<0.5 μM) and by the addition of ≥20 μM Zn2+. Sca permease-mediated uptake of 54Mn2+ was inhibited by Zn2+ but not by Ca2+, Mg2+, Fe2+, or Cu2+. Reduced uptake of54Mn2+ by sca mutants and by wild-type cells in the presence of Zn2+ was abrogated by the uncoupler carbonylcyanide m-chlorophenylhydrazone, suggesting that Mn2+ uptake under these conditions was proton motive force dependent. The frequency of DNA-mediated transformation was reduced >20-fold in sca mutants. The addition of 0.1 mM Mn2+ to the transformation medium restored only partly the transformability of mutant cells, implying an alternate role for Sca proteins in the transformation process. Cells ofsca mutants were unaffected in other binding properties tested and were unaffected in sensitivity to oxidants. The results show that Sca permease is a high-affinity mechanism for the acquisition of Mn2+ and is essential for growth of streptococci under Mn2+-limiting conditions.

The global transcriptional response of Bacillus subtilis to manganese involves the MntR, Fur, TnrA and σB regulons

“…These results suggest that Mn(II) uptake involves at least one additional system. In support of this model, ABC transporters for Mn(II) have been described in several bacterial species including Synechocystis 6803 ( Bartsevich and Pakrasi, 1995), Streptococcus gordonii (Kolenbrander et al ., 1998;Jakubovics et al ., 2000) and S. pneumoniae (Dintilhac and Claverys, 1997). More recently, S. enterica serovar Typhimurium, SitABCD was characterized as a Mn(II) transporter that operates optimally at alkaline pH whereas MntH functions optimally at acidic pH (Kehres et al ., 2002b).…”

Horizontal gene transfer and host specificity of beta‐haemolytic streptococci: the role of a putative composite transposon containing scpB and lmb

“…Lmb of S. agalactiae displays similarities to LraI proteins of other streptococci and mediates the binding to human laminin (Spellerberg et al, 1999). Besides their role in adhesion (Jenkinson, 1994;Berry and Paton, 1996;Viscount et al, 1997) LraI proteins have been shown to be involved in the transport of divalent cations (Dintilhac et al, 1997;Kolenbrander et al, 1998). However, a typical ABC transporter has not been found in the nucleotide sequence adjacent to the lmb locus, and the addition of manganese did not affect the growth of Lmb mutants (Spellerberg et al, 1999).…”

The solute‐binding component of a putative Mn(II) ABC transporter (MntA) is a novel Bacillus anthracis virulence determinant

“…A dual specificity in metal ion ABC transporters has been suggested in other studies. For example, investigation of metal ion transportdeficient mutants in S. gordonii (scaCBA), S. pneumoniae (psaBCA), S. mutans (sloABC) and S. parasanguis (fim-CBA) (Dintilhac et al, 1997;Kolenbrander et al, 1998;Oetjen et al, 2002;Janulczyk et al, 2003;Paik et al, 2003) showed that both manganese and ferrous ions can be bound and transported. These two ions are required by bacteria as enzyme cofactors and as structural components of proteins, but only manganese is known to participate in oxidative stress defence (Jakubovics and Jenkinson, 2001).…”