Structure and interactions of the archaeal motility repression module ArnA–ArnB that modulates archaellum gene expression in Sulfolobus acidocaldarius

Hoffmann, Lena; Anders, Katrin; Bischof, Lisa Franziska; Ye, Xing; Reimann, Julia; Khadouma, Sunia; Pham, Trong Khoa; Does, Chris van der; Wright, Phillip C.; Essen, Lars‐Oliver; Albers, Sonja‐Verena

doi:10.1074/jbc.ra119.007709

Cited by 19 publications

(32 citation statements)

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“…cells (Hoffmann et al, 2019). The C-terminal domain of ArnB could be phosphorylated by ArnC in vitro (Hoffmann et al, 2017) and was found phosphorylated in vivo, which suggested that phosphorylation/dephosphorylation of this domain might influence its interaction with ArnA (Hoffmann et al, 2019).…”

Section: Identification Of Proteins Associated With Ptp and Pp2amentioning

confidence: 99%

“…Deletion of arnR and arnR1 reduced flaB expression and impaired swimming motility. Previous experiments showed that ArnR and ArnR1 regulated the flaB promoter, but not the flaX promoter (Lassak et al, 2013;Bischof et al, 2019). AbfR1, an archaeal biofilm regulator, is also a positive regulator for archaellum expression and its binding to DNA is phosphorylation dependent (Orell et al, 2013;Li et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

“…The phosphorylation state of Tyr 84 and Ser 87 of AbfR1 regulates the interaction with its own promoter and the regulatory function in biofilm formation and motility (Li et al, 2017). In addition, a recent study indicated that the archaellum regulator ArnR and ArnR1 are phosphorylated by ArnC in vitro, however, whether the phosphorylation was involved in regulating their functions was not demonstrated yet (Bischof et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

“…These two proteins strongly interacted with each other both in vitro and in vivo . The expression of arnA and arnB is kept constant in cells, while their interaction sequentially diminished in nutrient starved cells ( Hoffmann et al, 2019 ). In S. tokodaii , ST0829, the homolog of ArnA, could bind to the flaX promoter region specifically ( Duan and He, 2011 ), which suggested that ArnA might be involved in the archaellum expression by binding to the promoters of the fla operon.…”

Section: Introductionmentioning

confidence: 99%

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The Phosphatase PP2A Interacts With ArnA and ArnB to Regulate the Oligomeric State and the Stability of the ArnA/B Complex

Vogt

Does

et al. 2020

Front. Microbiol.

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In the crenarchaeon Sulfolobus acidocaldarius, the archaellum, a type-IV pilus like motility structure, is synthesized in response to nutrient starvation. Synthesis of components of the archaellum is controlled by the archaellum regulatory network (arn). Protein phosphorylation plays an important role in this regulatory network since the deletion of several genes encoding protein kinases and the phosphatase PP2A affected cell motility. Several proteins in the archaellum regulatory network can be phosphorylated, however, details of how phosphorylation levels of different components affect archaellum synthesis are still unknown. To identify proteins interacting with the S. acidocaldarius phosphatases PTP and PP2A, co-immunoprecipitation assays coupled to mass spectrometry analysis were performed. Thirty minutes after growth in nutrient starvation medium, especially a conserved putative ATP/GTP binding protein (Saci_1281), a universal stress protein (Saci_0887) and the archaellum regulators ArnA and ArnB were identified as highly abundant interaction proteins of PP2A. The interaction between ArnA, ArnB, and PP2A was further studied. Previous studies showed that the Forkhead-associated domain containing ArnA interacts with von Willebrand type A domain containing ArnB, and that both proteins could be phosphorylated by the kinase ArnC in vitro. The ArnA/B heterodimer was reconstituted from the purified proteins. In complex with ArnA, phosphorylation of ArnB by the ArnC kinase was strongly stimulated and resulted in formation of (ArnA/B) 2 and higher oligomeric complexes, while association and dephosphorylation by PP2A resulted in dissociation of these ArnA/B complexes.

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Section: Identification Of Proteins Associated With Ptp and Pp2amentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The Phosphatase PP2A Interacts With ArnA and ArnB to Regulate the Oligomeric State and the Stability of the ArnA/B Complex

Vogt

Does

et al. 2020

Front. Microbiol.

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“…In bacteria, FHA-containing proteins were able to bind phosphorylated proteins ( Alderwick et al, 2006 ; Niebisch et al, 2006 ). In S. acidocaldarius , the interaction of FHA and vWA1 was mediated by phosphorylation and the cell motility was regulated by this interaction ( Reimann et al, 2012 ; Albers and Jarrell, 2015 ; Hoffmann et al, 2019 ; Ye et al, 2020 ). Our data suggested that vWA2 might also be phosphorylated and interacted with FHA in vivo .…”

Section: Resultsmentioning

confidence: 99%

Phosphoproteomic Analysis Reveals Rio1-Related Protein Phosphorylation Changes in Response to UV Irradiation in Sulfolobus islandicus REY15A

Huang

Lin

et al. 2020

Front. Microbiol.

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DNA damage response (DDR) in eukaryotes is largely regulated by protein phosphorylation. In archaea, many proteins are phosphorylated, however, it is unclear how the cells respond to DNA damage through global protein phosphorylation. We previously found that Δrio1, a Rio1 kinase homolog deletion strain of Sulfolobus islandicus REY15A, was sensitive to UV irradiation. In this study, we showed that Δrio1 grew faster than the wild type. Quantitative phosphoproteomic analysis of the wild type and Δrio1, untreated and irradiated with UV irradiation, revealed 562 phosphorylated sites (with a Ser/Thr/Tyr ratio of 65.3%/23.8%/10.9%) of 333 proteins in total. The phosphorylation levels of 35 sites of 30 proteins changed with >1.3-fold in the wild type strain upon UV irradiation. Interestingly, more than half of the UV-induced changes in the wild type did not occur in the Δrio1 strain, which were mainly associated with proteins synthesis and turnover. In addition, a protein kinase and several transcriptional regulators were differentially phosphorylated after UV treatment, and some of the changes were dependent on Rio1. Finally, many proteins involved in various cellular metabolisms exhibited Riol-related and UV-independent phosphorylation changes. Our results suggest that Rio1 is involved in the regulation of protein recycling and signal transduction in response to UV irradiation, and plays regulatory roles in multiple cellular processes in S. islandicus.

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Archaellum

Jarrell¹,

Tripp²,

Albers³

2020

Encyclopedia of Life Sciences

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Each of the three domains of life contains its own unique swimming apparatus. The archaellum (formerly called archaeal flagellum) is a unique, ‘tail‐like’ structure used for motility by single‐celled organisms belonging to the domain Archaea. Although archaella are functionally similar to the flagella found on bacteria, they differ significantly in structure and mode of assembly. Archaella are evolutionarily related to type IV pili, and each of the two systems shares several key homologues required for assembly of the respective structures. Recent studies have contributed much to our knowledge concerning the regulation of the operon encoding the archaellum proteins. In addition, the elucidation of the structures of most of the Fla proteins involved in archaella structure and function, coupled with detailed atomic models of the archaellum, including the motor, has provided major insights into how this unique motility organelle is assembled and functions, often in harsh environments inhabited by many archaea. Key Concepts Each of the three domains of life has a unique motility apparatus, which have recently been assigned distinct names (Archaea: archaellum; Bacteria: flagellum and Eukaryotes: cilium). The archaellum is functionally equivalent to flagellum but is evolutionarily related to a type IV pilus, with the archaella and type IV pili systems sharing important homologues. Archaea have the ability to regulate the synthesis of archaella depending on growth conditions, such as available nutrients and temperature. There can be crosstalk in the regulation of archaella with adhesive pili, allowing the cells under certain conditions to make only one type of appendage, either for swimming or adhesion. N‐Glycosylation of the major filament proteins, the archaellins, is widespread and essential under normal conditions for assembly of filaments. The ATPase responsible for assembly of the archaellins into the filament, that is, FlaI, is also responsible for the hydrolysis of ATP that powers the rotation of archaella. In many archaea, the archaellum interacts with a bacterial‐like chemotaxis system that requires novel chemotaxis proteins to act as adaptors to connect the systems. Not all archaellated species have an associated chemotaxis system. Knowledge of the structure and assembly of archaella has greatly increased in the past 5 years with atomic models of several archaella structures as well as structures of most of the individual archaella proteins and their interaction partners.

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Structure and interactions of the archaeal motility repression module ArnA–ArnB that modulates archaellum gene expression in Sulfolobus acidocaldarius

Cited by 19 publications

References 47 publications

The Phosphatase PP2A Interacts With ArnA and ArnB to Regulate the Oligomeric State and the Stability of the ArnA/B Complex

The Phosphatase PP2A Interacts With ArnA and ArnB to Regulate the Oligomeric State and the Stability of the ArnA/B Complex

Phosphoproteomic Analysis Reveals Rio1-Related Protein Phosphorylation Changes in Response to UV Irradiation in Sulfolobus islandicus REY15A

Archaellum

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