Gene expression of terminal oxidases in two marine bacterial strains exposed to nanomolar oxygen concentrations

Abstract

The final step of aerobic respiration is carried out by a terminal oxidase transporting electrons to oxygen (O2). Prokaryotes harbor diverse terminal oxidases that differ in phylogenetic origin, structure, biochemical function, and affinity for O2. Here we report on the expression of high-affinity (cytochrome cbb3 oxidase), low-affinity (cytochrome aa3 oxidase), and putative low-affinity (cyanide-insensitive oxidase (CIO)) terminal oxidases in the marine bacteria Idiomarina loihiensis L2-TR and Marinobacter daepoensis SW-156 upon transition to very low O2 concentrations (<200 nM), measured by RT-qPCR. In both strains, high-affinity cytochrome cbb3 oxidase showed the highest expression levels and was significantly up-regulated upon transition to low O2 concentrations. Low-affinity cytochrome aa3 oxidase showed very low transcription levels throughout the incubation. Surprisingly, however, it was also up-regulated upon transition to low O2 concentrations. In contrast, putative low-affinity CIO had much lower expression levels and markedly different regulation patterns between the two strains. These results demonstrate that exposure to low O2 concentrations regulates the gene expression of different types of terminal oxidases, but also that the type and magnitude of transcriptional response is species-dependent. Therefore, in situ transcriptome data cannot, without detailed knowledge of the transcriptional regulation of the species involved, be translated into relative respiratory activity.

Microaerobic Lifestyle at Nanomolar O 2 Concentrations Mediated by Low-Affinity Terminal Oxidases in Abundant Soil Bacteria

“…S1b ). A continuous expression of low-affinity caa 3 -type TOs at low O 2 concentrations was previously reported in aerobic marine bacterial species ( 19 , 49 ); however, in that study ( 19 ), the high-affinity cbb 3 -type TO was upregulated at <0.2 μmol O 2 liter −1 . In our study, we did not observe any measurable contribution via transcriptomics or qPCR of the high-affinity cbb 3 -type TO in any of the strains at 10 to 0.001 μmol O 2 liter −1 , although we cannot completely rule out the possibility of a minor contribution (undetectable with our current methods) of the cbb 3 -type TO.…”

“…At nanomolar O 2 concentrations, microorganisms transition from aerobic respiration to anaerobic-based metabolism (substrate-level phosphorylation or anaerobic respiration), referred to as the Pasteur point ( 17 , 18 ). To the best of our knowledge, gene expression-based investigations of terminal oxidases at nanomolar O 2 concentrations are scarce (e.g., Gong et al reported expression at O 2 levels of ≤200 nmol [ 19 ]), and therefore, it is mostly speculated that the high-affinity terminal oxidases are primarily responsible for energy production at low-nanomolar O 2 concentrations.…”

Freshwater carbon and nutrient cycles revealed through reconstructed population genomes

“…Cytochrome c oxidases, both aa3- and cbb3-type, were widespread in all three lake environments and frequently co-occurred within MAGs. aa3-type cytochromes are associated with high oxygen concentrations, while cbb3-type cytochromes are associated with low oxygen concentrations (Gong et al, 2018). The presence of genes encoding both types suggests the flexibility to operate under a range of oxygen concentrations.…”

Influences of Seasonal Monsoons on the Taxonomic Composition and Diversity of Bacterial Community in the Eastern Tropical Indian Ocean

“…Biogeochemical characteristics, including temperature, nutrients, salinity, and DO, are the important regulators of bacterial community composition in many marine ecosystems (Biddanda et al, 2001;Naqvi, 2006;Paulmier and Ruiz-Pino, 2009;Guo et al, 2018;Gao et al, 2020). The temperature of surface water in the Indian Ocean is closely related to the seasonal variation of the monsoon.…”