The Terminal Oxidase cbb ₃ Functions in Redox Control of Magnetite Biomineralization in Magnetospirillum gryphiswaldense

Abstract

The biomineralization of magnetosomes in Magnetospirillum gryphiswaldense and other magnetotactic bacteria occurs only under suboxic conditions. However, the mechanism of oxygen regulation and redox control of biosynthesis of the mixed-valence iron oxide magnetite [FeII(FeIII) 2 O 4 ] is still unclear. Here, we set out to investigate the role of aerobic respiration in both energy metabolism and magnetite biomineralization of M. gryphiswaldense. Although three operons encoding putative terminal cbb 3 -type, aa 3 -type, and bd-type oxidases were identified in the genome assembly of M. gryphiswaldense, genetic and biochemical analyses revealed that only cbb 3 and bd are required for oxygen respiration, whereas aa 3 had no physiological significance under the tested conditions. While the loss of bd had no effects on growth and magnetosome synthesis, inactivation of cbb 3 caused pleiotropic effects under microaerobic conditions in the presence of nitrate. In addition to their incapability of simultaneous nitrate and oxygen reduction, cbb 3 -deficient cells had complex magnetosome phenotypes and aberrant morphologies, probably by disturbing the redox balance required for proper growth and magnetite biomineralization. Altogether, besides being the primary terminal oxidase for aerobic respiration, cbb 3 oxidase may serve as an oxygen sensor and have a further role in poising proper redox conditions required for magnetite biomineralization.

Transcriptome analysis reveals physiological characteristics required for magnetosome formation in Magnetospirillum gryphiswaldense MSR‐1

“…Each of the TFs examined regulates multiple genes, and conversely specific genes are regulated by more than one TF, consistent with the complexity of the proposed regulatory network for cellular metabolic processes. Among the candidate regulators, functions and regulated genes of transcriptional factor MGMSRv2_3137 (Qi et al ., ; Deng et al ., ), MGMSRv2_2946 (Li et al ., ) and MGMSRv2_2046 have been preliminary researched. The predicted regulatory network of this study provides another interesting regulated genes for these regulators.…”

“…MSR-1 has two other terminal oxidase operons that include ccoNOQP (MGMSRv2_2954-MGMSRv2_2951) and cydAB (MGMSRv2_3972-MGMSRv2_3970). Two types of cytochrome c oxidases, Cta oxidases and Cco oxidases, belong respectively to the aa 3 and cbb 3 family (Li et al, 2014b). The two types of complexes accept electrons from ubiquinone, transferred by cytochrome cb 1 PetABC (ubiquinol-cytochrome c reductase complex) and cytochrome c protein (Dibrova et al, 2013).…”

Overproduction of Magnetosomes by Genomic Amplification of Biosynthesis-Related Gene Clusters in a Magnetotactic Bacterium

“…Surprisingly, increasing the extracellular iron levels beyond this concentration had no effect on biomineralization in the overproducing strains, and chromosomal duplication of genes encoding the ferrous iron transporter FeoAB1 also had only minor effects (Table 2), indicating that the iron supply is not a limiting factor for magnetite overproduction under the tested conditions. However, biomineralization of the mixed-valence iron oxide magnetite was found to be critically dependent on a proper ferric-to-ferrous iron ratio (44)(45)(46), and thus, regulation by general metabolic pathways such as aerobic and anaerobic respiration processes might become limiting with increasing expression levels of the magnetosome synthesis machinery.…”

An Aerobic Exercise: Defining the Roles of Pseudomonas aeruginosa Terminal Oxidases

“…cbb 3 oxidase purified from Pseudomonas stutzeri has been shown to have NOR activity (22), and the cbb 3 oxidases of P. aeruginosa have been implicated in anaerobic denitrification and NO-mediated effects on biofilm formation (17). In diverse organisms, effects of the cbb 3 oxidases on the expression of other metabolic genes and on biomineralization have suggested that they may be involved in sensing and responding to changes in redox homeostasis (4,23,24). Finally, results from the current study and others suggest that modulation of the P. aeruginosa respiratory chain is strongly influenced by environmental stresses, and the different oxidases provide activity under distinct, specialized conditions (6,7,16).…”