Differential effect of YidC depletion on the membrane proteome of Escherichia coli under aerobic and anaerobic growth conditions

Abstract

YidC of Escherichia coli belongs to the evolutionarily conserved Oxa1/Alb3/YidC family. Members of the family have all been implicated in membrane protein biogenesis of respiratory and energy transducing proteins. The number of proteins identified thus far to require YidC for their membrane biogenesis remains limited and the identification of new substrates may allow the elucidation of properties that define the YidC specificity. To this end we investigated changes in the membrane proteome of E. coli upon YidC depletion using metabolic labeling of proteins with 15N/14N combined with a MS-centered proteomics approach and compared the effects of YidC depletion under aerobic and anaerobic growth conditions. We found that YidC depletion resulted in protein aggregation/misfolding in the cytoplasm as well as in the inner membrane of E. coli. A dramatic increase was observed in the chaperone-mediated stress response upon YidC depletion and this response was limited to aerobically grown cells. A number of transporter proteins were identified as possible candidates for the YidC-dependent insertion and/or folding pathway. These included the small metal ion transporter CorA, numerous ABC transporters, as well as the MFS transporters KgtP and ProP, providing a new subset of proteins potentially requiring YidC for membrane biogenesis.

Biogenesis of YidC Cytoplasmic Membrane Substrates Is Required for Positioning of Autotransporter IcsA at Future Poles

“…Data from recent studies suggest that 17 to 32% of cytoplasmic membrane proteins depend on YidC for proper assembly (20,21). In cells that lack YidC, proteins that are YidC substrates either fail to insert into the membrane or are inserted but improperly assembled.…”

“…For a subset of these proteins, biogenesis depends on the cytoplasmic membrane insertase YidC (Oxa1p) (15)(16)(17)(18)(19)(20)(21). YidC (Oxa1p) is widely conserved, with homologs in other bacteria, Archaea, mitochondria, and chloroplasts (22,23); thus, its role in membrane protein biogenesis is relevant to all living organisms.…”

Role of the Cytosolic Loop C2 and the C Terminus of YidC in Ribosome Binding and Insertion Activity

“…Depletion of YidC also impairs cell growth under anaerobic conditions cause by defects in the membrane biogenesis of the anaerobic respiratory complexes, such as NADH dehydrogenase and the F 1 F 0 ATPase (43). To determine whether the designed YidC variants could fulfill the growth complementation function under anaerobic conditions, E. coli strain FTL10 harboring the genes encoding for YidC variants were grown in anaerobic medium supplemented with 0.5% w/v glycerol and 10 mM sodium fumarate serving as the nonfermentable carbon source and electron acceptor, respectively.…”

Identification of Putative Substrates for the Periplasmic Chaperone YfgM in Escherichia coli Using Quantitative Proteomics

“…Interestingly, IbpA and IbpB are also higher in abundance in strains lacking proteins involved in translocation and targeting across the inner membrane (i.e. SecB, SecE, and YidC) (35)(36)(37).…”