An electron transfer path connects subunits of a mycobacterial respiratory supercomplex

Gong, Haiming; Li, Jun; Xu, Ao; Tang, Yanting; Ji, Wenxin; Gao, Ruogu; Wang, Shuhui; Yu, Lu; Tian, Chong‐Bin; Li, Jingwen; Yen, Hsin‐Yung; Lam, Sin Man; Shui, Guanghou; Yang, Xiuna; Sun, Yuna; Li, Xuemei; Jia, Minghao; Yang, Cheng; Jiang, Biao; Lou, Zhiyong; Robinson, Carol V.; Wong, Luet‐Lok; Guddat, Luke W.; Sun, Fei; Wang, Quan; Rao, Zihe

doi:10.1126/science.aat8923

Cited by 129 publications

(230 citation statements)

References 93 publications

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“…The actinobacteria have a membrane‐associated dihaem cytochrome c (Bott and Niebisch, ) rather than the typical soluble cytochrome c , which usually functions to shuttle electrons between complexes III and IV in the respiratory chain (Nicholls and Ferguson, ). In the actinobacteria, complex III (cytochrome bcc oxidoreductase) and complex IV (cytochrome aa 3 oxidase) form a supercomplex through which electrons are channelled, with protein–protein interactions being critical to the process (Gong et al ., ; Wiseman et al ., ). Due to the dependence of Nar1 on the presence of the supercomplex, this suggests the intriguing possibility that Nar1 might transiently associate with this supercomplex in spores to divert electrons to the NarG1 catalytic subunit when O 2 concentrations drop below a critical threshold (< 5 μM; Falke et al ., ).…”

Section: Nitrate Respiration At the Hypoxic‐anoxic Interfacementioning

confidence: 99%

Anaerobic nitrate respiration in the aerobe Streptomyces coelicolor A3(2): helping maintain a proton gradient during dormancy

Sawers

Fischer

Falke

2019

Environ Microbiol Rep

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Summary Respiratory nitrate reductases (Nar) catalyse the reduction of nitrate to nitrite, coupling this process to energy conservation. The obligate aerobic actinobacterium Streptomyces coelicolor synthesizes three Nar enzymes that contribute to maintenance of a membrane potential when either the mycelium or the spores become hypoxic or anoxic. No growth occurs under such conditions but the bacterium survives the lack of O2 by remaining metabolically active; reducing nitrate is one means whereby this process is aided. Nar1 is exclusive to spores, Nar2 to vegetative mycelium and Nar3 to stationary‐phase mycelium, each making a distinct contribution to energy conservation. While Nar2 and Nar3 appear to function like conventional menaquinol oxidases, unusually, Nar1 is completely dependent for its activity on a cytochrome bcc‐aa 3 oxidase supercomplex. This suggest that electrons within this supercomplex are diverted to Nar1 during O2 limitation. Receiving electrons from this supercomplex potentially allows nitrate reduction to be coupled to the Q‐cycle of the cytochrome bcc complex. This modification likely improves the efficiency of energy conservation, extending longevity of spores under O2 limitation. Knowledge gained on the bioenergetics of NO3− respiration in the actinobacteria will aid our understanding of how many microorganisms survive under conditions of extreme nutrient and energy restriction.

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Section: Nitrate Respiration At the Hypoxic‐anoxic Interfacementioning

confidence: 99%

Anaerobic nitrate respiration in the aerobe Streptomyces coelicolor A3(2): helping maintain a proton gradient during dormancy

Sawers

Fischer

Falke

2019

Environ Microbiol Rep

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“…Unlike the obligate CIII 2 CIV 2 SC of Actinobacteria, which is rigid and devoid of a free electron carrier (Gong et al, 2018;Wiseman et al, 2018), the R. capsulatus facultative CIII 2 CIV is naturally of low abundance and flexible, limiting its structural resolution. The dual function of bacterial CIII 2 interacting with both the photochemical reaction center in photosynthesis, and cyt c oxidase in respiration, may necessitate this natural plasticity to allow swift metabolic adaptations.…”

Section: Discussionmentioning

confidence: 99%

“…Mitochondrial SCs, such as CICIII 2 CIV (respirasomes) or their smaller variants containing only CICIII 2 (Sousa and Vonck, 2019) or CIII 2 CIV (Letts et al, 2016) have established molecular architectures Hartley et al, 2019;Wu et al, 2016). Bacterial SCs, including these of P. denitrificans (Berry and Trumpower, 1985;Stroh et al, 2004), Geobacillus stearothermophilus (Bergdoll et al, 2016), Bacillus PS3 (Sone et al, 1987), M. smegmatis (Kim et al, 2015), and C. glutamicum (Kao et al, 2016), have been characterized biochemically, but only the structure of the Gram positive M. smegmatis SC (CIII 2 CIV 2 ) has been reported (Gong et al, 2018;Wiseman et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Cryo-EM Structures of Respiratorybc₁-cbb₃type CIII₂CIV Supercomplex and Electronic Communication Between the Complexes

Steimle

Eeuwen

Öztürk

et al. 2020

Preprint

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The respiratory electron transport complexes convey electrons from nutrients to oxygen and generate a proton-motive force used for energy (ATP) production in cells. These enzymes are conserved among organisms, and organized as individual complexes or combined forming large super-complexes (SC). Bacterial electron transport pathways are more branched than those of mitochondria and contain multiple variants of such complexes depending on their growth modes. The Gram-negative species deploy a mitochondrial-like cytochrome bc1 (Complex III, CIII2), and may have bacteria-specific cbb3-type cytochrome c oxidases (Complex IV, CIV) in addition to, or instead of, the canonical aa3-type CIV. Electron transfer between these complexes is mediated by two different carriers: the soluble cytochrome c2 which is similar to mitochondrial cytochrome c and the membrane-anchored cytochrome cy which is unique to bacteria. Here, we report the first cryo-EM structure of a respiratory bc1-cbb3 type SC (CIII2CIV, 5.2Å resolution) and several conformers of native CIII2 (3.3Å resolution) from the Gram-negative bacterium Rhodobacter capsulatus. The SC contains all catalytic subunits and cofactors of CIII2 and CIV, as well as two extra transmembrane helices attributed to cytochrome cy and the assembly factor CcoH. Remarkably, some of the native CIII2 are structural heterodimers with different conformations of their [2Fe-2S] cluster-bearing domains. The unresolved cytochrome c domain of cy suggests that it is mobile, and it interacts with CIII2CIV differently than cytochrome c2. Distance requirements for electron transfer suggest that cytochrome cy and cytochrome c2 donate electrons to heme cp1 and heme cp2 of CIV, respectively. For the first time, the CIII2CIV architecture and its electronic connections establish the structural features of two separate respiratory electron transport pathways (membrane-confined and membrane-external) between its partners in Gram-negative bacteria.

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“…Total lipids were extracted from the samples using an improved Bligh/Dyer extraction method (double extraction) and appropriate internal standards were added as previously described [17]. Analysis of mycolic acids and lipids was carried out using normal-phase LC-MS as previously described, with minor modi cation [35,36]. The experiments were conducted with the help of Lipidall Technologies Company Limited (Changzhou, Jiangsu, China).…”

Section: Analysis Of the Composition Of Mycolic Acids And Lipids Usinmentioning

confidence: 99%

The aceE involves in mycolic acid synthesis and biofilm formation in Mycobacterium smegmatis

Chen

Teng

Wen

et al. 2020

Preprint

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Background: The integrity of cell wall structure is highly significant for the in vivo survival of mycobacteria. We hypothesized that changes in morphology may indicate changes in cell wall metabolism and identified an aceE gene mutant ( aceE -mut) which presented a deficient colony morphology on 7H10 agar by screening transposon mutagenesis in Mycolicibacterium smegmatis , basonym Mycobacterium smegmatis ( M. smegmatis ). This study aimed to identify the functional role of aceE gene in cell wall biosynthesis in M. smegmatis. Results: We observed that the colony morphology of aceE -mut was quite different, smaller and smoother on the solid culture medium than the wild-type (WT) strain during the transposon library screening of M. smegmatis . Notably, in contrast with the WT, which aggregates and forms biofilm, the aceE -mut lost its ability of growing aggregately and biofilm formation, which are two very important features of mycobacteria. The morphological changes in the aceE -mut strain were further confirmed by electron microscopy which indicated smoother and thinner cell envelope images in contrast with the rough morphology of WT strains. Additionally, the aceE -mut was more fragile to acidic stress and exhibited a pronounced defects in entering the macrophages as compared to the WT. The analysis of mycolic acid (MA) using LC-MS indicated deficiency of alpha-MA and epoxy-MA in aceE -mut strain whereas complementation of the aceE -mut with a wild-type aceE gene restored the composition of MA. Conclusions: Over all, this study indicates that aceE gene plays a significant role in the mycolic acid synthesis and affects the colony morphology, biofilm formation of M. smegmatis and bacteria invasion of macrophage.

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An electron transfer path connects subunits of a mycobacterial respiratory supercomplex

Cited by 129 publications

References 93 publications

Anaerobic nitrate respiration in the aerobe Streptomyces coelicolor A3(2): helping maintain a proton gradient during dormancy

Anaerobic nitrate respiration in the aerobe Streptomyces coelicolor A3(2): helping maintain a proton gradient during dormancy

Cryo-EM Structures of Respiratorybc₁-cbb₃type CIII₂CIV Supercomplex and Electronic Communication Between the Complexes

The aceE involves in mycolic acid synthesis and biofilm formation in Mycobacterium smegmatis

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An electron transfer path connects subunits of a mycobacterial respiratory supercomplex

Cited by 129 publications

References 93 publications

Anaerobic nitrate respiration in the aerobe Streptomyces coelicolor A3(2): helping maintain a proton gradient during dormancy

Anaerobic nitrate respiration in the aerobe Streptomyces coelicolor A3(2): helping maintain a proton gradient during dormancy

Cryo-EM Structures of Respiratorybc1-cbb3type CIII2CIV Supercomplex and Electronic Communication Between the Complexes

The aceE involves in mycolic acid synthesis and biofilm formation in Mycobacterium smegmatis

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Cryo-EM Structures of Respiratorybc₁-cbb₃type CIII₂CIV Supercomplex and Electronic Communication Between the Complexes