The nucleotide‐dependent interaction of FlaH and FlaI is essential for assembly and function of the archaellum motor

Chaudhury, Paushali; Neiner, Tomasz; D’Imprima, Edoardo; Banerjee, Ankan; Reindl, Sophia; Ghosh, Abhrajyoti; Arvai, A.S.; Mills, Deryck J.; Does, Chris van der; Tainer, John A.; Vonck, Janet; Albers, Sonja‐Verena

doi:10.1111/mmi.13260

Cited by 52 publications

(119 citation statements)

References 38 publications

(65 reference statements)

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“…The same considerations apply to branch A3, which includes KaiC-like proteins with two active ATPase domains. The third branch (A17) that appears to be ancestral consists of FlaH proteins, essential archaellum components (36,45). The remaining tree branches are either lineage specific or include only a few archaeal lineages ( Table 2; Table S3).…”

Section: Resultsmentioning

confidence: 99%

“…The multiple lines of evidence discussed above indicate that the KaiC family is likely a major hub of a versatile and complex archaeal signaling network that so far has largely escaped attention. Nevertheless, the available experimental data on a halobacterial circadian clock (24,57) and the recent progress in the study of the functions of FlaH in the archaellum (35,36,45) allow us to propose two models of the roles of KaiC-like proteins in signal transduction (Fig. 4).…”

Section: Resultsmentioning

confidence: 99%

“…1C), has been solved and shown to be similar to the C-terminal domain of KaiC (35,36). FlaH has been shown to form a hexamer and interact with the archaellum subunit FlaI, the motor ATPase, and in crenarchaea, with the FlaX ring (35,36). KaiC family ATPase GvpD was found to be involved in the regulation of Halobacterium-specific gas vesicles (37) (Fig.…”

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confidence: 99%

“…Recently, the structure of the FlaH protein (COG2874 family), which is always encoded within the archaellum operon (Fig. 1C), has been solved and shown to be similar to the C-terminal domain of KaiC (35,36). FlaH has been shown to form a hexamer and interact with the archaellum subunit FlaI, the motor ATPase, and in crenarchaea, with the FlaX ring (35,36).…”

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confidence: 99%

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Proposed Role for KaiC-Like ATPases as Major Signal Transduction Hubs in Archaea

Makarova

Galperin

Koonin

2017

mBio

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All organisms must adapt to ever-changing environmental conditions and accordingly have evolved diverse signal transduction systems. In bacteria, the most abundant networks are built around the two-component signal transduction systems that include histidine kinases and receiver domains. In contrast, eukaryotic signal transduction is dominated by serine/threonine/tyrosine protein kinases. Both of these systems are also found in archaea, but they are not as common and diversified as their bacterial and eukaryotic counterparts, suggesting the possibility that archaea have evolved other, still uncharacterized signal transduction networks. Here we propose a role for KaiC family ATPases, known to be key components of the circadian clock in cyanobacteria, in archaeal signal transduction. The KaiC family is notably expanded in most archaeal genomes, and although most of these ATPases remain poorly characterized, members of the KaiC family have been shown to control archaellum assembly and have been found to be a stable component of the gas vesicle system in Halobacteria. Computational analyses described here suggest that KaiC-like ATPases and their homologues with inactivated ATPase domains are involved in many other archaeal signal transduction pathways and comprise major hubs of complex regulatory networks. We predict numerous input and output domains that are linked to KaiC-like proteins, including putative homologues of eukaryotic DEATH domains that could function as adapters in archaeal signaling networks. We further address the relationships of the archaeal family of KaiC homologues to the bona fide KaiC of cyanobacteria and implications for the existence of a KaiCbased circadian clock apparatus in archaea.IMPORTANCE Little is currently known about signal transduction pathways in Archaea. Recent studies indicate that KaiC-like ATPases, known as key components of the circadian clock apparatus in cyanobacteria, are involved in the regulation of archaellum assembly and, likely, type IV pili and the gas vesicle system in Archaea. We performed comprehensive comparative genomic analyses of the KaiC family. A vast protein interaction network was revealed, with KaiC family proteins as hubs for numerous input and output components, many of which are shared with twocomponent signal transduction systems. Putative KaiC-based signal transduction systems are predicted to regulate the activities of membrane-associated complexes and individual proteins, such as signal recognition particle and membrane transporters, and also could be important for oxidative stress response regulation. KaiC-centered signal transduction networks are predicted to play major roles in archaeal physiology, and this work is expected to stimulate their experimental characterization.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

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confidence: 99%

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Proposed Role for KaiC-Like ATPases as Major Signal Transduction Hubs in Archaea

Makarova

Galperin

Koonin

2017

mBio

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“…These different orientations are necessary to computationally generate a 3D, high-resolution density map of the sample. This technique has recently been used to visualize the interaction of the archaellar core protein FlaH inside a ring of FlaX in vitro (54).…”

Section: Expanding the Toolboxmentioning

confidence: 99%

Recent Advances and Future Prospects in Bacterial and Archaeal Locomotion and Signal Transduction

et al. 2017

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The structure and function of two-component and chemotactic signaling and different aspects related to the motility of bacteria and archaea are key research areas in modern microbiology. Escherichia coli is the traditional model organism used to study chemotaxis signaling and motility. However, the recent study of a wide range of bacteria and even some archaea with different lifestyles has provided new insight into the ecophysiology of chemotaxis, which is essential for the establishment of different pathogens or beneficial bacteria in a host. The expanded range of model organisms has also permitted the study of chemosensory pathways unrelated to chemotaxis, multiple chemotaxis pathways within an organism, and new types of chemoreceptors. This research has greatly benefitted from technical advances in the field of cryomicroscopy, which continues to reveal with increasing resolution the complexity and diversity of large protein complexes like the flagellar motor or chemoreceptor arrays. In addition, sensitive instruments now allow an increasing number of experiments to be conducted at the single-cell level, thereby revealing information that is beginning to bridge the gap between individual cells and population behavior. Evidence has also accumulated showing that bacteria have evolved different mechanisms for surface sensing, which appears to be mediated by flagella and possibly type IV pili, and that the downstream signaling involves chemosensory pathways and two-component-system-based processes. Herein, we summarize the recent advances and research tendencies in this field as presented at the latest Bacterial Locomotion and Signal Transduction (BLAST XIV) conference.KEYWORDS chemotaxis, flagella, flagellar motility, signal transduction, two-component regulatory systems T he capacity to sense and respond to changes in environmental cues is an essential feature of the prokaryotic lifestyle. As a consequence, bacteria and archaea have evolved an array of different molecular mechanisms that permit the detection of signals in order to generate appropriate cellular responses. These responses are mediated primarily by one-and two-component systems, as well as chemosensory signaling pathways (1-4). Whereas the former systems mediate changes primarily at the transcriptional level, chemosensory pathways form the basis for chemotaxis, the directed movement of prokaryotes in compound gradients. The study of signaling processes is not only of fundamental interest but may also contribute to the tackling of one of the central clinical problems, which is the increasing amount of antibiotic-resistant pathogens. There is now a significant amount of data indicating that interference with signal transduction systems, motility, and chemotaxis can be an alternative strategy to weaken or block pathogens (5, 6).In

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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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The nucleotide‐dependent interaction of FlaH and FlaI is essential for assembly and function of the archaellum motor

Cited by 52 publications

References 38 publications

Proposed Role for KaiC-Like ATPases as Major Signal Transduction Hubs in Archaea

Proposed Role for KaiC-Like ATPases as Major Signal Transduction Hubs in Archaea

Recent Advances and Future Prospects in Bacterial and Archaeal Locomotion and Signal Transduction

Archaellum

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