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Review
. 2021 Nov 23;45(6):fuab028.
doi: 10.1093/femsre/fuab028.

Regulation and distinct physiological roles of manganese in bacteria

Elleke F Bosma  1 , Martin H Rau  1 , Lieke A van Gijtenbeek  1 , Solvej Siedler  1
Affiliations
Review

Regulation and distinct physiological roles of manganese in bacteria

Elleke F Bosma et al. FEMS Microbiol Rev. .

Abstract

Manganese (Mn2+) is an essential trace element within organisms spanning the entire tree of life. In this review, we provide an overview of Mn2+ transport and the regulation of its homeostasis in bacteria, with a focus on its functions beyond being a cofactor for enzymes. Crucial differences in Mn2+ homeostasis exist between bacterial species that can be characterized to have an iron- or manganese-centric metabolism. Highly iron-centric species require minimal Mn2+ and mostly use it as a mechanism to cope with oxidative stress. As a consequence, tight regulation of Mn2+ uptake is required, while organisms that use both Fe2+ and Mn2+ need other layers of regulation for maintaining homeostasis. We will focus in detail on manganese-centric bacterial species, in particular lactobacilli, that require little to no Fe2+ and use Mn2+ for a wider variety of functions. These organisms can accumulate extraordinarily high amounts of Mn2+ intracellularly, enabling the nonenzymatic use of Mn2+ for decomposition of reactive oxygen species while simultaneously functioning as a mechanism of competitive exclusion. We further discuss how Mn2+ accumulation can provide both beneficial and pathogenic bacteria with advantages in thriving in their niches.

Keywords: bacilli; competitive exclusion; lactobacilli; manganese; oxidative stress.

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Figures

Figure 1.
Figure 1.
Functions of Mn2+ in bacteria. From left to right, the organisms become more manganese centric and use Mn2+ for an increasing number of cellular functions of which they share the ones depicted as overlapping boxes; the two depicted separately at the very right have very specialized functions for Mn2+ that are not shared by other species. The species given in the top row are the most-studied examples, but the traits are not necessarily exclusive to these species.
Figure 2.
Figure 2.
Manganese transporters in bacteria. For presence and absence of the different transporters and their regulation, see Table S1 (Supporting Information) and Figs 3–5. Note that the nomenclature for the ABC transporter differs per species. Throughout this review, we will refer to it as MntABC, but other names are SloABC, MtsABC and SitABC (or CBA). Figure based on Bane (2015).
Figure 3.
Figure 3.
Manganese transport and regulation in the iron-centric E. coli. The individual transcriptional regulators are depicted at the top, including their mechanisms, e.g. metal binding, as well as in the figure to indicate their binding sites. For MntR, an additional symbol for the DNA binding site (BS-mntR) in light blue has been chosen for clarity. Repression and activation symbols indicate the influence of the individual transcription factors shown above upon Mn2+ addition. Genes are depicted in thick arrows and transcription start sites are shown in thin arrows. The base pair (bp) numbers indicate the distance from the gene to the transcription start site. The 2D structure of folded RNA is depicted with and without Mn2+ addition. The coding regions of mntR and mntP are shown in green and lilac, respectively, while the upstream region is shown in gray.
Figure 4.
Figure 4.
Manganese transport and regulation in B. subtilis(A) and Streptococcusoligofermentans(B), which require both Fe2+ and Mn2+ and hence are neither iron- nor manganese centric. MntR homodimer is depicted in light blue and its regulation, e.g. metal binding, and H2O2 availability, are shown at the top. A thick, light blue line represents the DNA binding site. Genes are depicted in thick arrows and transcription start sites are shown in thin arrows. Repression and activation symbols indicate the influence of the individual transcription factors shown above upon Mn2+ addition. The base pair (bp) numbers indicate the distance from the gene to the transcription start site. The 2D structure of folded RNA is depicted with and without Mn2+ addition.
Figure 5.
Figure 5.
Manganese transport and regulation in the manganese-centric L. plantarum. MntR homodimer is depicted in light blue and a thick light blue line represents the DNA binding site. Genes are depicted in thick arrows and transcription start sites are shown in thin arrows. Repression and activation symbols indicate the influence of the individual transcription factors shown above upon manganese access conditions. The base pair (bp) numbers indicate the distance from the gene to the transcription start site. MntH* represents the Mn2+ transporter that has been shown to be responsible for competitive exclusion (Siedler et al. 2020), while MntH# depicts the regulation of the additional one to two mntH genes. No MntR binding site was found in front of mntH# or mntR, but responsiveness upon Mn2+ addition or depletion was shown experimentally. Mn2+ concentrations from low to very high are depicted below with the indicated repression or activation symbol to depict the regulation. The responsible regulatory element has not been identified yet. Note that mntH1 and mntH2 in the papers of Tong et al. (2017a,b) are two subunits of the ABC transporter based on primer sequence and hence depicted and named here as such.
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