Insights into the mechanism and regulation of the CbbQO-type Rubisco activase, a MoxR AAA+ ATPase

Tsai, Yi-Chin Candace; Ye, Fuzhou; Liew, Lynette; Liu, Di; Bhushan, Shashi; Gao, Yong‐Gui; Mueller‐Cajar, Oliver

doi:10.1073/pnas.1911123117

Cited by 34 publications

(52 citation statements)

References 53 publications

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“…The close proximity of genes encoding an AAA ATPase and a vWA-MIDAS domain protein has been reported in thermophilic archaeal viruses, such as Acidianus Two-Tailed Virus (ATV) [ 54 ]. The interaction between AAA ATPase and a vWA-MIDAS domain protein has been closely studied in several cases, and a common finding is that the vWA-MIDAS domain protein provides an adaptor function, while the AAA ATPase acts as a chaperone [ 55 , 56 ].…”

Section: Resultsmentioning

confidence: 99%

The Novel Halovirus Hardycor1, and the Presence of Active (Induced) Proviruses in Four Haloarchaea

Dyall‐Smith

Pfeiffer

Chiang

et al. 2021

Genes

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The virus Hardycor1 was isolated in 1998 and infects the haloarchaeon Halorubrum coriense. DNA from a frozen stock (HC1) was sequenced and the viral genome found to be 45,142 bp of dsDNA, probably having redundant, circularly permuted termini. The genome showed little similarity (BLASTn) to known viruses. Only twenty-two of the 53 (41%) predicted proteins were significantly similar to sequences in the NCBI nr protein database (E-value ≤ 10−15). Six caudovirus-like proteins were encoded, including large subunit terminase (TerL), major capsid protein (Mcp) and tape measure protein (Tmp). Hardycor1 was predicted to be a siphovirus (VIRFAM). No close relationship to other viruses was found using phylogenetic tree reconstructions based on TerL and Mcp. Unexpectedly, the sequenced virus stock HC1 also revealed two induced proviruses of the host: a siphovirus (Humcor1) and a pleolipovirus (Humcor2). A re-examination of other similarly sequenced, archival virus stocks revealed induced proviruses of Haloferax volcanii, Haloferax gibbonsii and Haloarcula hispanica, three of which were pleolipoviruses. One provirus (Halfvol2) of Hfx. volcanii showed little similarity (BLASTn) to known viruses and probably represents a novel virus group. The attP sequences of many pleolipoproviruses were found to be embedded in a newly detected coding sequence, split in the provirus state, that spans between genes for integrase and a downstream CxxC-motif protein. This gene might play an important role in regulation of the temperate state.

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Section: Resultsmentioning

confidence: 99%

The Novel Halovirus Hardycor1, and the Presence of Active (Induced) Proviruses in Four Haloarchaea

Dyall‐Smith

Pfeiffer

Chiang

et al. 2021

Genes

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“…This MIDAS-mediated mechanism may be a more general alternative strategy utilized by a subclass of AAA proteins. One example is the MoxR-group AAA protein CbbQ, a Rubisco activase that requires a MIDAS-containing cofactor protein to function (32)(33)(34). Recent structural work has shown that the MIDAScontaining von Willebrand factor A (VWA) domain of this cofactor docks onto the hexameric AAA ring of CbbQ in a bimolecular interaction, and furthermore that the VWA domain communicates information about substrate binding to the AAA ring (32).…”

Section: Discussionmentioning

confidence: 99%

Long-range intramolecular allostery and regulation in the dynein-like AAA protein Mdn1

Mickolajczyk

Olinares

Niu

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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Mdn1 is an essential mechanoenzyme that uses the energy from ATP hydrolysis to physically reshape and remodel, and thus mature, the 60S subunit of the ribosome. This massive (>500 kDa) protein has an N-terminal AAA (ATPase associated with diverse cellular activities) ring, which, like dynein, has six ATPase sites. The AAA ring is followed by large (>2,000 aa) linking domains that include an ∼500-aa disordered (D/E-rich) region, and a C-terminal substrate-binding MIDAS domain. Recent models suggest that intramolecular docking of the MIDAS domain onto the AAA ring is required for Mdn1 to transmit force to its ribosomal substrates, but it is not currently understood what role the linking domains play, or why tethering the MIDAS domain to the AAA ring is required for protein function. Here, we use chemical probes, single-particle electron microscopy, and native mass spectrometry to study the AAA and MIDAS domains separately or in combination. We find that Mdn1 lacking the D/E-rich and MIDAS domains retains ATP and chemical probe binding activities. Free MIDAS domain can bind to the AAA ring of this construct in a stereo-specific bimolecular interaction, and, interestingly, this binding reduces ATPase activity. Whereas intramolecular MIDAS docking appears to require a treatment with a chemical inhibitor or preribosome binding, bimolecular MIDAS docking does not. Hence, tethering the MIDAS domain to the AAA ring serves to prevent, rather than promote, MIDAS docking in the absence of inducing signals.

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“…In contrast the CbbQO-type Rca found in chemoautotrophic proteobacteria consists of a cup-shaped AAA+ hexamer (CbbQ 6) bound to a single adaptor protein CbbO, which is essential for Rubisco activation (9). During Rca function the hexamer remodels CbbO, which is bound to inhibited Rubisco via a von Willebrand Factor A domain (16).…”

Section: Introductionmentioning

confidence: 99%

Rubisco activase requires residues in the large subunit N terminus to remodel inhibited plant Rubisco

Guo

Mueller‐Cajar

2020

Journal of Biological Chemistry

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The photosynthetic CO2 fixing enzyme ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco) forms dead-end inhibited complexes while binding multiple sugar phosphates, including its substrate ribulose 1,5-bisphosphate. Rubisco can be rescued from this inhibited form by molecular chaperones belonging to the ATPases associated with diverse cellular activities (AAA+ proteins) termed Rubisco activases (Rcas). The mechanism of green-type Rca found in higher plants has proved elusive, in part because until recently higher plant Rubiscos could not be expressed recombinantly. Identifying the interaction sites between Rubisco and Rca is critical to formulate mechanistic hypotheses. Towards that end here we purify and characterize a suite of 33 Arabidopsis Rubisco mutants for their ability to be activated by Rca. Mutation of 17 surface-exposed large subunit residues did not yield variants that were perturbed in their interaction with Rca. In contrast, we find that Rca activity is highly sensitive to truncations and mutations in the conserved N-terminus of the Rubisco large subunit. Large subunits lacking residues 1-4 are functional Rubiscos, but cannot be activated. Both T5A and T7A substitutions result in functional carboxylases that are poorly activated by Rca, indicating the side chains of these residues form a critical interaction with the chaperone. Many other AAA+ proteins function by threading macromolecules through a central pore of a disc-shaped hexamer. Our results are consistent with a model where Rca transiently threads the Rubisco large subunit N-terminus through the axial pore of the AAA+ hexamer.

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Insights into the mechanism and regulation of the CbbQO-type Rubisco activase, a MoxR AAA+ ATPase

Cited by 34 publications

References 53 publications

The Novel Halovirus Hardycor1, and the Presence of Active (Induced) Proviruses in Four Haloarchaea

The Novel Halovirus Hardycor1, and the Presence of Active (Induced) Proviruses in Four Haloarchaea

Long-range intramolecular allostery and regulation in the dynein-like AAA protein Mdn1

Rubisco activase requires residues in the large subunit N terminus to remodel inhibited plant Rubisco

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