Regulation and distinct physiological roles of manganese in bacteria

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 co-factor for enzymes. Crucial differences in Mn2+ homeostasis exist between bacterial species that can be characterized to have 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 non-enzymatic 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.

Calcium determines Lactiplantibacillus plantarum intraspecies competitive fitness

“…Despite having similar total quantities of metals in cMRS, B1.3 still contained lower amounts of magnesium, aluminum, and calcium compared to strain B1.1. Presently, aside from a few reports suggesting different metal requirements for lactobacilli (27)(28)(29)(30)(31), the importance of metals for LAB growth and ecological interactions are not well understood. The requirement of L. plantarum for manganese has been specifically investigated (30,32), likely because L. plantarum has a high requirement for Mn 2+ compared to other bacteria and Mn 2+ is known to confer resistance against oxidative (33,34) and heat (35) stress.…”

“…Presently, aside from a few reports suggesting different metal requirements for lactobacilli (27)(28)(29)(30)(31), the importance of metals for LAB growth and ecological interactions are not well understood. The requirement of L. plantarum for manganese has been specifically investigated (30,32), likely because L. plantarum has a high requirement for Mn 2+ compared to other bacteria and Mn 2+ is known to confer resistance against oxidative (33,34) and heat (35) stress. However, the potentially overlapping effects of metal cations (36) on L. plantarum and other lactobacilli remain to be determined.…”

ZccE is a Novel P-type ATPase That Protects Streptococcus mutans Against Zinc Intoxication

“…As both Zn and Mn are linked to oxidative stress responses (50)(51)(52), we sought to determine if simultaneous perturbations of Zn and Mn homeostasis (and therefore of Zn:Mn ratios) in ∆zccE affected the ability of this strain to cope with peroxide stress. In disc diffusion assays, both UA159…”

Manganese Stress Adaptation Mechanisms of Bacillus safensis Strain ST7 From Mine Soil

“…Furthermore, Mn is an essential trace element for all living organisms, acting as a cofactor for many enzymes, such as oxidoreductases, transferases, ligases, and hydrolases ( Wang et al, 2019 ). Mn also participates in oxidative stress resistance, metabolism and decomposition of reactive oxygen species (ROS) ( Bosma et al, 2021 ), and is required for the development and function of nerve and immune cells, control of blood sugar and vitamin levels in animals, and photosynthesis and respiration processes in plants ( Gao et al, 2014 ). However, consumption of food or drinking water containing a high level of Mn has undesirable effects on human health ( O’Neal and Zheng, 2015 ).…”