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Title: Cyanobacterial carboxysomes contain an unique rubisco-activase-like protein

Abstract

In plants, rubisco activase (Rca) regulates rubisco by removing inhibitory molecules such as ribulose–1,5–bisphosphate (RuBP). In cyanobacteria, a homologous protein (activase–like cyanobacterial protein, ALC), contains a distinctive C–terminal fusion resembling the small–subunit of rubisco. Although cyanobacterial rubisco is believed to be less sensitive to RuBP inhibition, the ALC is widely distributed among diverse cyanobacteria. Using microscopy, biochemistry and molecular biology, the cellular localization of the ALC, its effect on carboxysome/cell ultrastructure in Fremyella diplosiphon, and its function in vitro were studied. Bioinformatic analysis uncovered evolutionary relationships between the ALC and rubisco. ALC localizes to carboxysomes and exhibits ATPase activity. Furthermore, the ALC induces rubisco aggregation in a manner similar to that of another carboxysomal protein, M35, and this activity is affected by ATP. An alc deletion mutant showed modified cell morphology when grown under enriched CO2 and impaired regulation of carboxysome biogenesis, without affecting growth rate. Carbamylation of Fremyella recombinant rubisco was inhibited by RuBP, but this inhibition was not relieved by the ALC. Here, the ALC does not appear to function like a canonical Rca; instead, it exerts an effect on the response to CO2 availability at the level of a metabolic module, the carboxysome, through rubisco network formation,more » and carboxysome organization.« less

Authors:
ORCiD logo [1]; ORCiD logo [1];  [1];  [1]; ORCiD logo [1]; ORCiD logo [2]
  1. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
  2. Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Publication Date:
Research Org.:
Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Laboratory
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1735821
Alternate Identifier(s):
OSTI ID: 1572105; OSTI ID: 1671328
Grant/Contract Number:  
FG02-91ER20021; FG02‐91ER20021
Resource Type:
Accepted Manuscript
Journal Name:
New Phytologist
Additional Journal Information:
Journal Volume: 225; Journal Issue: 2; Journal ID: ISSN 0028-646X
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; carboxysome; cyanobacteria; Fremyella diplosiphon; rubisco; rubisco activase

Citation Formats

Lechno‐Yossef, Sigal, Rohnke, Brandon A., Belza, Ana O., Melnicki, Matthew R., Montgomery, Beronda L., and Kerfeld, Cheryl A. Cyanobacterial carboxysomes contain an unique rubisco-activase-like protein. United States: N. p., 2019. Web. doi:10.1111/nph.16195.
Lechno‐Yossef, Sigal, Rohnke, Brandon A., Belza, Ana O., Melnicki, Matthew R., Montgomery, Beronda L., & Kerfeld, Cheryl A. Cyanobacterial carboxysomes contain an unique rubisco-activase-like protein. United States. https://doi.org/10.1111/nph.16195
Lechno‐Yossef, Sigal, Rohnke, Brandon A., Belza, Ana O., Melnicki, Matthew R., Montgomery, Beronda L., and Kerfeld, Cheryl A. Fri . "Cyanobacterial carboxysomes contain an unique rubisco-activase-like protein". United States. https://doi.org/10.1111/nph.16195. https://www.osti.gov/servlets/purl/1735821.
@article{osti_1735821,
title = {Cyanobacterial carboxysomes contain an unique rubisco-activase-like protein},
author = {Lechno‐Yossef, Sigal and Rohnke, Brandon A. and Belza, Ana O. and Melnicki, Matthew R. and Montgomery, Beronda L. and Kerfeld, Cheryl A.},
abstractNote = {In plants, rubisco activase (Rca) regulates rubisco by removing inhibitory molecules such as ribulose–1,5–bisphosphate (RuBP). In cyanobacteria, a homologous protein (activase–like cyanobacterial protein, ALC), contains a distinctive C–terminal fusion resembling the small–subunit of rubisco. Although cyanobacterial rubisco is believed to be less sensitive to RuBP inhibition, the ALC is widely distributed among diverse cyanobacteria. Using microscopy, biochemistry and molecular biology, the cellular localization of the ALC, its effect on carboxysome/cell ultrastructure in Fremyella diplosiphon, and its function in vitro were studied. Bioinformatic analysis uncovered evolutionary relationships between the ALC and rubisco. ALC localizes to carboxysomes and exhibits ATPase activity. Furthermore, the ALC induces rubisco aggregation in a manner similar to that of another carboxysomal protein, M35, and this activity is affected by ATP. An alc deletion mutant showed modified cell morphology when grown under enriched CO2 and impaired regulation of carboxysome biogenesis, without affecting growth rate. Carbamylation of Fremyella recombinant rubisco was inhibited by RuBP, but this inhibition was not relieved by the ALC. Here, the ALC does not appear to function like a canonical Rca; instead, it exerts an effect on the response to CO2 availability at the level of a metabolic module, the carboxysome, through rubisco network formation, and carboxysome organization.},
doi = {10.1111/nph.16195},
journal = {New Phytologist},
number = 2,
volume = 225,
place = {United States},
year = {2019},
month = {10}
}

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Figures / Tables:

Fig. 1 Fig. 1: Phylogenetic analysis of cyanobacterial ALC and RbcL sequences. (a) Unrooted phylogeny of AAA+ domains of activase‐like cyanobacterial proteins (ALCs) and rubisco activase (Rca) sequences. The AAA+ domain of 133 ALC sequences was identified in 374 cyanobacterial genomes, aligned with 10 plant and algal Rca reference sequences, and usedmore » for phylogenetic tree construction. (b) Phylogeny of Form IB rubisco large subunit (RbcL) and correspondence with ALC subtypes. RbcL sequences from 335 cyanobacterial genomes were aligned with 13 plant and algal representatives, used for phylogenetic tree construction, and were rooted by the Form IA rubisco sequences from alpha‐cyanobacteria (subclade C1, shown collapsed). Vertical bars depict the phylogenetic subclades of the host genomes (based on Shih et al., 2013). Columns at right show correspondence with ALC subtypes when present in the same genome. (c) Unrooted phylogenetic tree comparing small subunit‐like domains (SSLDs) from CcmM (179 domains in 51 CcmM sequences) and ALC (56 representative sequences) with RbcS (56 representative sequences).« less

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Works referencing / citing this record:

Binding Options for the Small Subunit-Like Domain of Cyanobacteria to Rubisco
journal, February 2020

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