Structural characterization of hexameric shell proteins from two types of choline-utilization bacterial microcompartments

Ochoa, Jessica M; Mijares, Oscar; Acosta, Andrea; Escoto, Xavier; Leon-Rivera, Nancy; Marshall, Joanna D.; Sawaya, M.R.; Yeates, Todd O.

doi:10.1107/s2053230x21007470

Cited by 3 publications

(3 citation statements)

References 47 publications

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“…PCC 7418 or BMC-H Hoch empty shells, both inside cells [19,38] or in vitro [39], while BMC-T presence was dispensable for the formation of minimalist α-carboxysomes [40] or Klebsiella pneumoniae GRM2 shells [41]. In the last study, CmcC from GRM2 was proposed to be a component endowed with high spontaneous curvature, in agreement with the crystal Arr-A organization of the E. coli K25A CmcC homolog [42]. Future studies are necessary to investigate the potential implication of BMC-T in mediating BMC-H assembly transitions, also to establish the physiological consequences that would have the alteration of the natural biogenesis pathway of a given BMC.…”

Section: Discussionsupporting

confidence: 53%

“…In the last study, CmcC from GRM2 was proposed to be a component endowed with high spontaneous curvature, in agreement with the crystal Arr-A organization of the E . coli K25A CmcC homolog [ 42 ]. Future studies are necessary to investigate the potential implication of BMC-T in mediating BMC-H assembly transitions, also to establish the physiological consequences that would have the alteration of the natural biogenesis pathway of a given BMC.…”

Section: Discussionmentioning

confidence: 99%

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Inferring assembly-curving trends of bacterial micro-compartment shell hexamers from crystal structure arrangements

et al. 2023

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Bacterial microcompartments (BMC) are complex macromolecular assemblies that participate in varied chemical processes in about one fourth of bacterial species. BMC-encapsulated enzymatic activities are segregated from other cell contents by means of semipermeable shells, justifying why BMC are viewed as prototype nano-reactors for biotechnological applications. Herein, we undertook a comparative study of bending propensities of BMC hexamers (BMC-H), the most abundant shell constituents. Published data show that some BMC-H, like β-carboxysomal CcmK, tend to assemble flat whereas other BMC-H often build curved objects. Inspection of available crystal structures presenting BMC-H in tiled arrangements permitted us to identify two major assembly modes with a striking connection with experimental trends. All-atom molecular dynamics (MD) supported that BMC-H bending is triggered robustly only from the arrangement adopted in crystals by BMC-H that experimentally form curved objects, leading to very similar arrangements to those found in structures of recomposed BMC shells. Simulations on triplets of planar-behaving hexamers, which were previously reconfigured to comply with such organization, confirmed that bending propensity is mostly defined by the precise lateral positioning of hexamers, rather than by BMC-H identity. Finally, an interfacial lysine was pinpointed as the most decisive residue in controlling PduA spontaneous curvature. Globally, results presented herein should contribute to improve our understanding of the variable mechanisms of biogenesis characterized for BMC, and of possible strategies to regulate BMC size and shape.

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Section: Discussionsupporting

confidence: 53%

Section: Discussionmentioning

confidence: 99%

Inferring assembly-curving trends of bacterial micro-compartment shell hexamers from crystal structure arrangements

et al. 2023

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show abstract

“…PCC 7418 or BMC-H Hoch empty shells, both inside cells 16, 37 or in vitro 38 , while BMC-T presence was dispensable for the formation of RMM-H Msm nanotubes 38 , minimalist α-carboxysomes 39 or Klebsiella pneumoniae GRM2 shells 40 . In the last study, cmcC from GRM2 was proposed to be a component endowed with high spontaneous curvature, in agreement with the crystal Ass-A organization of the E. coli K25A cmcC homolog 41 . Future studies will be required to address the possible implication of BMC-T in mediating BMC-H assembly transitions, also to investigate the physiological consequences of altering the natural biogenesis pathway of a given BMC.…”

Section: Discussionsupporting

confidence: 65%

Inferring assembly-curving trends of bacterial micro-compartment shell hexamers from crystal structure arrangements

Garcia-Alles

Soldan

Custovic³

et al. 2022

Preprint

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Bacterial microcompartments (BMC) are complex macromolecular assemblies that participate to varied chemical processes in about one fourth of bacterial species. BMC-encapsulated enzymatic activities are segregated from other cell contents by means of semipermeable shells, justifying why BMC are viewed as prototype nano-reactors for biotechnological applications. Herein, we undertook a comparative study of trends of self-assembly of BMC hexamers (BMC-H), the most abundant shell constituents. Published and new microscopy data show that some BMC-H, likeβ-carboxysomal CcmK, tend to assemble flat whereas other BMC-H often build curved-implying objects. Inspection of available crystal structures presenting BMC-H in tiled arrangements permitted to identify two major assembly modes with a striking connection with experimental trends. All-atom molecular dynamics (MD) supported that BMC-H bending is triggered robustly only from the disposition adopted by BMC-H that form curved objects experimentally, conducting to almost identical arrangements to those found in structures of recomposed BMC shells. Simulations on ensembles of planar-behaving hexamers, which were previously reconfigured to comply with such disposition, confirmed that bending is defined by assembly details, rather than by BMC-H identity. Finally, although no common atomic determinants could be identified as responsible of BMC-H spontaneous curvature, an inter-hexamer ionic pair was pinpointed as contributor to hold a subset of BMC-H in low bending dispositions. These results are expected to improve our understanding of the variable mechanisms of biogenesis characterized for BMC, and of possible strategies to regulate BMC size and shape.

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Ethanolamine-induced assembly of microcompartments is required forFusobacterium nucleatumvirulence

Franklin,

Chen,

Chen

et al. 2024

Preprint

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Many bacteria metabolize ethanolamine as a nutrient source through cytoplasmic organelles named bacterial microcompartments (BMCs). Here we investigated the molecular assembly, regulation, and function of BMCs inFusobacterium nucleatum– a Gram-negative oral pathobiont that is associated with adverse pregnancy outcomes. TheF. nucleatumgenome harbors a conserved ethanolamine utilization (eut) locus with 21 genes that encode several putative BMC shell proteins and a two-component signal transduction system (TCS), in addition to the enzymes for ethanolamine transport and catabolism. We show that the expression of most of these genes as well as BMC formation is highly increased in wild type fusobacteria when cultured in the presence of ethanolamine as a nutrient source. Deletion of the response regulator EutV eliminated this induction ofeutmRNAs and BMCs, thus demonstrating that BMC formation is transcriptionally regulated by the TCS EutV-EutW in response to ethanolamine. Mass spectrometry of isolated BMCs unveiled the identity of the constituent proteins EutL, EutM1, EutM2, and EutN. Consistent with the role of these proteins in BMC assembly and metabolism, deletion ofeutN,eutL/eutM1/eutM2, oreutL/eutM1/eutM2/eutNnot only affected BMC formation, but also ethanolamine utilization, causing cell growth defects with ethanolamine as nutrient. BMCs also assembled in fusobacteria cultured with placental cells or the culture media, a process that is dependent on the BMC shell proteins. Significantly, we show that theeutNmutant is defective in inducing preterm birth in a mouse model. Together, these results establish that BMC-mediated metabolism of ethanolamine is critical for fusobacterial virulence.

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Structural characterization of hexameric shell proteins from two types of choline-utilization bacterial microcompartments

Cited by 3 publications

References 47 publications

Inferring assembly-curving trends of bacterial micro-compartment shell hexamers from crystal structure arrangements

Inferring assembly-curving trends of bacterial micro-compartment shell hexamers from crystal structure arrangements

Inferring assembly-curving trends of bacterial micro-compartment shell hexamers from crystal structure arrangements

Ethanolamine-induced assembly of microcompartments is required forFusobacterium nucleatumvirulence

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