Microbes occupy diverse and often extreme environments that encounter constant challenges, including fluctuating resource availability. As microbes frequently obtain nutrients from the extracellular environment, their survival is often reliant on metabolic flexibility. Consequently, many microbes have unique enzymes that drive respiration and energy generation.
Like all organisms, microbes rely on adenosine triphosphate (ATP) to power cellular processes. The key site of ATP generation for aerobic microbes is the membrane-associated respiratory chain. The respiratory chain couples the oxidation of fuel compounds to the reduction of terminal electron acceptors, such as oxygen, via specific membrane-localised respiratory enzymes. The transfer of electrons in this process generates energy that produces an electrochemical gradient that powers ATP synthesis via ATP synthase. Integral to this are membrane-localised respiratory quinones that carry electrons between these respiratory enzymes.
As the microbial membrane is a site of numerous cellular processes, area on the membrane is highly sought-after. Here, I present a novel strategy microbes employ to overcome membrane congestion and promote metabolic flexibility. The strategy, called long-range quinone transport, uses a specialised family of proteins we termed Respiratory Chain Coupling Proteins (RCCPs).
Employing genomic surveys and phylogenetic analysis, we found that RCCPs are widespread in bacteria and archaea and are associated to varied respiratory enzymes. Through four high-resolution cryo-EM structures and structural modelling we show that RCCPs form a tetrameric protein tube that have an internal hydrophobic chamber and externally scaffold respiratory enzymes. Further, through molecular dynamics simulations, biochemical and physiological experiments we show that the RCCP tube interacts transiently with the membrane to extract quinones into the hydrophobic chamber. The quinones are then delivered to the associated enzymes for electron transfer, allowing for respiration in the cytoplasm. Our findings demonstrate that long-range quinone transport is an essential driver of microbial respiration, promoting metabolic flexibility and microbial survival.