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Carboxysomes, responsible for a substantial fraction of CO 2 fixation on Earth, are proteinaceous microcompartments found in many autotrophic members of domain Bacteria , primarily from the phyla Proteobacteria and Cyanobacteria . Carboxysomes facilitate CO 2 fixation by the Calvin-Benson-Bassham (CBB) cycle, particularly under conditions where the CO 2 concentration is variable or low, or O 2 is abundant. These microcompartments are composed of an icosahedral shell containing the enzymes ribulose 1,5-carboxylase/oxygenase (RubisCO) and carbonic anhydrase. They function as part of a CO 2 concentrating mechanism, in which cells accumulate HCO 3 − in the cytoplasm via active transport, HCO 3 − enters the carboxysomes through pores in the carboxysomal shell proteins, and carboxysomal carbonic anhydrase facilitates the conversion of HCO 3 − to CO 2 , which RubisCO fixes. Two forms of carboxysomes have been described: α-carboxysomes and β-carboxysomes, which arose independently from ancestral microcompartments. The α-carboxysomes present in Proteobacteria and some Cyanobacteria have shells comprised of four types of proteins [CsoS1 hexamers, CsoS4 pentamers, CsoS2 assembly proteins, and α-carboxysomal carbonic anhydrase (CsoSCA)], and contain form IA RubisCO (CbbL and CbbS). In the majority of cases, these components are encoded in the genome near each other in a gene locus, and transcribed together as an operon. Interestingly, genome sequencing has revealed some α-carboxysome loci that are missing genes encoding one or more of these components. Some loci lack the genes encoding RubisCO, others lack a gene encoding carbonic anhydrase, some loci are missing shell protein genes, and in some organisms, genes homologous to those encoding the carboxysome-associated carbonic anhydrase are the only carboxysome-related genes present in the genome. Given that RubisCO, assembly factors, carbonic anhydrase, and shell proteins are all essential for carboxysome function, these absences are quite intriguing. In this review, we provide an overview of the most recent studies of the structural components of carboxysomes, describe the genomic context and taxonomic distribution of atypical carboxysome loci, and propose functions for these variants. We suggest that these atypical loci are JEEPs, which have modified functions based on the presence of Just Enough Essential Parts.
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A new type of carboxysomal carbonic anhydrase in sulfur chemolithoautotrophs from alkaline environments
ABSTRACT Autotrophic bacteria are able to fix CO2in a great diversity of habitats, even though this dissolved gas is relatively scarce at neutral pH and above. As many of these bacteria rely on CO2fixation by ribulose 1,5-bisphospate carboxylase/oxygenase (RubisCO) for biomass generation, they must compensate for the catalytical constraints of this enzyme with CO2-concentrating mechanisms (CCMs). CCMs consist of CO2and HCO3−transporters and carboxysomes. Carboxysomes encapsulate RubisCO and carbonic anhydrase (CA) within a protein shell and are essential for the operation of a CCM in autotrophicBacteriathat use the Calvin-Benson-Basham cycle. Members of the genusThiomicrospiralack genes homologous to those encoding previously described CA, and prior to this work, the mechanism of function for their carboxysomes was unclear. In this paper, we provide evidence that a member of the recently discovered iota family of carbonic anhydrase enzymes (ιCA) plays a role in CO2fixation by carboxysomes from members ofThiomicrospiraand potentially otherBacteria. Carboxysome enrichments fromThiomicrospira pelophilaandThiomicrospira aerophilawere found to have CA activity and contain ιCA, which is encoded in their carboxysome loci. When the gene encoding ιCA was interrupted inT. pelophila, cells could no longer grow under low-CO2conditions, and CA activity was no longer detectable in their carboxysomes. WhenT. pelophilaιCA was expressed in a strain ofEscherichia colilacking native CA activity, this strain recovered an ability to grow under low CO2conditions, and CA activity was present in crude cell extracts prepared from this strain. IMPORTANCEHere, we provide evidence that iota carbonic anhydrase (ιCA) plays a role in CO2fixation by some organisms with CO2-concentrating mechanisms; this is the first time that ιCA has been detected in carboxysomes. While ιCA genes have been previously described in other members of bacteria, this is the first description of a physiological role for this type of carbonic anhydrase in this domain. Given its distribution in alkaliphilic autotrophic bacteria, ιCA may provide an advantage to organisms growing at high pH values and could be helpful for engineering autotrophic organisms to synthesize compounds of industrial interest under alkaline conditions.
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- Award ID(s):
- 1930451
- PAR ID:
- 10543510
- Editor(s):
- Biddle, Jennifer F
- Publisher / Repository:
- American Society for Microbiology
- Date Published:
- Journal Name:
- Applied and Environmental Microbiology
- Volume:
- 90
- Issue:
- 9
- ISSN:
- 0099-2240
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1128/aem.01075-24
