Electron transport and protein secretion pathways involved in Mn(III) reduction by Shewanella oneidensis

Abstract

Soluble Mn(III) represents an important yet overlooked oxidant in marine and freshwater systems. The molecular mechanism of microbial Mn(III) reduction, however, has yet to be elucidated. Extracellular reduction of insoluble Mn(IV) and Fe(III) oxides by the metal-reducing γ-proteobacterium Shewanella oneidensis involves inner (CymA) and outer (OmcA) membrane-associated c-type cytochromes, the extracellular electron conduit MtrCAB, and GspD, the secretin of type II protein secretion. CymA, MtrCAB and GspD mutants were unable to reduce Mn(III) and Mn(IV) with lactate, H2, or formate as electron donor. The OmcA mutant reduced Mn(III) and Mn(IV) at near wild-type rates with lactate and formate as electron donor. With H2 as electron donor, however, the OmcA mutant was unable to reduce Mn(III) but reduced Mn(IV) at wild-type rates. Analogous Fe(III) reduction rate analyses indicated that other electron carriers compensated for the absence of OmcA, CymA, MtrCAB and GspD during Fe(III) reduction in an electron donor-dependent fashion. Results of the present study demonstrate that the S. oneidensis electron transport and protein secretion components involved in extracellular electron transfer to external Mn(IV) and Fe(III) oxides are also required for electron transfer to Mn(III) and that OmcA may function as a dedicated component of an H2 oxidation-linked Mn(III) reduction system.

Functional roles of CymA and NapC in reduction of nitrate and nitrite by Shewanella putrefaciens W3-18-1

“…As shown previously, CymA, a central part of electron transfer pathways that support respiratory flexibility of Shewanella, functions as an electron-transfer hub in anaerobic respiration (Cordova et al, 2011;Marritt et al, 2012a, b). CymA can support the reduction of many electron acceptors, such as nitrate, nitrite, fumarate, DMSO,Fe 3+ , Mn 4+ , Cr 4+ and arsenate (Fonseca et al, 2013;McMillan et al, 2012;Murphy & Saltikov, 2007;Szeinbaum et al, 2014). Also, it has recently been shown that CymA is essential for selenite reduction by S. oneidensis MR-1 (Li et al, 2014).…”

Microbial manganese(III) reduction fuelled by anaerobic acetate oxidation

“…The other described route for acetate oxidation is the oxidative acetyl‐CoA pathway (Wood‐Ljungdahl pathway) (Hori et al ., ; Ticak et al ., ), but the absence of genes encoding the acetyl‐CoA synthase/carbon monoxide dehydrogenase complex (Supporting Information Table S2) renders this pathway unlikely in Shewanella . Strain MN‐01 also encodes the complete mtr pathway necessary for Mn 3+ reduction in Shewanella (Szeinbaum et al ., ). Based on our comparative genomic analysis, and considering that both C1 and C2 from acetate are oxidized to CO 2 , we propose that in S. algae , acetate oxidation during Mn 3+ reduction proceeds via the complete dehydrogenase‐driven TCA cycle, perhaps using the SSDH bypass that Cyanobacteria employ as an obligate route.…”

Physiological and transcriptional approaches reveal connection between nitrogen and manganese cycles in Shewanella algae C6G3

“…6) with fumarate as a control. Mn(IV) reduction is performed in two steps (i) reduction of Mn(IV) to Mn(III) and (ii) reduction of Mn(III) to Mn 2+ , both steps seem to be dependent on the Mtr system, but only the second step causes CO 2 -production42.…”