Archaeal Signal Transduction: Impact of Protein Phosphatase Deletions on Cell Size, Motility, and Energy Metabolism in Sulfolobus acidocaldarius

Reimann, Julia; Esser, Dominik; Orell, Alvaro; Amman, Fabian; Pham, Trong Khoa; Noirel, Josselin; Lindås, Ann-Christin; Bernander, Rolf; Wright, Phillip C.; Siebers, Bettina; Albers, Sonja‐Verena

doi:10.1074/mcp.m113.027375

Cited by 52 publications

(125 citation statements)

References 79 publications

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“…In contrast, we could not identify any connections between the KaiC-centered network and genes involved in the S/T kinase pathway. Additionally, inspection of the available data on archaeal phosphoproteomes yielded no indications of extensive phosphorylation of KaiC pathway-related genes (62)(63)(64). Thus, the KaiC network appears to be largely disjointed from the S/T kinase-mediated regulatory pathways in Archaea.…”

Section: Resultsmentioning

confidence: 98%

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: 98%

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

Makarova

Galperin

Koonin

2017

mBio

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“…tokodaii, are the best-studied Archaea regarding protein phosphorylation. Four protein phosphatases (427)(428)(429) and five protein kinases (430)(431)(432)(433)(434) were identified and biochemically investigated. Furthermore, the first signal transduction pathway involved in archaella expression mediated by reversible protein phosphorylation was discovered in Sul.…”

Section: Regulation At the Protein Levelmentioning

confidence: 99%

“…Furthermore, the first signal transduction pathway involved in archaella expression mediated by reversible protein phosphorylation was discovered in Sul. acidocaldarius (429,435) and Sul. tokodaii (436).…”

Section: Regulation At the Protein Levelmentioning

confidence: 99%

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Carbohydrate Metabolism in Archaea: Current Insights into Unusual Enzymes and Pathways and Their Regulation

Bräsen

Esser

Rauch

et al. 2014

Microbiol Mol Biol Rev

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294

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SUMMARY The metabolism of Archaea , the third domain of life, resembles in its complexity those of Bacteria and lower Eukarya . However, this metabolic complexity in Archaea is accompanied by the absence of many “classical” pathways, particularly in central carbohydrate metabolism. Instead, Archaea are characterized by the presence of unique, modified variants of classical pathways such as the Embden-Meyerhof-Parnas (EMP) pathway and the Entner-Doudoroff (ED) pathway. The pentose phosphate pathway is only partly present (if at all), and pentose degradation also significantly differs from that known for bacterial model organisms. These modifications are accompanied by the invention of “new,” unusual enzymes which cause fundamental consequences for the underlying regulatory principles, and classical allosteric regulation sites well established in Bacteria and Eukarya are lost. The aim of this review is to present the current understanding of central carbohydrate metabolic pathways and their regulation in Archaea . In order to give an overview of their complexity, pathway modifications are discussed with respect to unusual archaeal biocatalysts, their structural and mechanistic characteristics, and their regulatory properties in comparison to their classic counterparts from Bacteria and Eukarya . Furthermore, an overview focusing on hexose metabolic, i.e., glycolytic as well as gluconeogenic, pathways identified in archaeal model organisms is given. Their energy gain is discussed, and new insights into different levels of regulation that have been observed so far, including the transcript and protein levels (e.g., gene regulation, known transcription regulators, and posttranslational modification via reversible protein phosphorylation), are presented.

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“…The genes were considered up-and down-regulated when their transcripts were log 2 (treated/reference) >1 or <À1. (Hiller et al, 2003) as well as three terminal oxidases: DoxBCE, SoxABCDL and the SoxM complex (Reimann et al, 2013). SoxABCDL oxidase and the SoxM complex are linked to oxygen availability (Simon et al, 2009) while the SoxM complex may also play a role in pH sensing (Komorowski et al, 2002).…”

Section: Rna Transcripts As a Response To Removal Of Either Potassiummentioning

confidence: 99%

Transcriptomic analysis reveals how a lack of potassium ions increases Sulfolobus acidocaldarius sensitivity to pH changes

et al. 2016

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Extremely acidophilic microorganisms (optimum growth pH of 3) maintain a near neutral cytoplasmic pH via several homeostatic mechanisms, including an inside positive membrane potential created by potassium ions. Transcriptomic responses to pH stress in the thermoacidophilic archaeon, Sulfolobus acidocaldarius were investigated by growing cells without added sodium and/or potassium ions at both optimal and sub-optimal pH. Culturing the cells in the absence of added sodium or potassium ions resulted in a reduced growth rate compared to full-salt conditions as well as 43 and 75 significantly different RNA transcript ratios, respectively. Differentially expressed RNA transcripts during growth in the absence of added sodium ions included genes coding for permeases, a sodium/proline transporter and electron transport proteins. In contrast, culturing without added potassium ions resulted in higher RNA transcripts for similar genes as a lack of sodium ions plus genes related to spermidine that has a general role in response to stress and a decarboxylase that potentially consumes protons. The greatest RNA transcript response occurred when S. acidocaldarius cells were grown in the absence of potassium and/or sodium at a sub-optimal pH. These adaptations included those listed above plus osmoregulated glucans and mechanosensitive channels that have previously been shown to respond to osmotic stress. In addition, data analyses revealed two co-expressed IclR family transcriptional regulator genes with a previously unknown role in the S. acidocaldarius pH stress response. Our study provides additional evidence towards the importance of potassium in acidophile growth at acidic pH.

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Archaeal Signal Transduction: Impact of Protein Phosphatase Deletions on Cell Size, Motility, and Energy Metabolism in Sulfolobus acidocaldarius

Cited by 52 publications

References 79 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

Carbohydrate Metabolism in Archaea: Current Insights into Unusual Enzymes and Pathways and Their Regulation

Transcriptomic analysis reveals how a lack of potassium ions increases Sulfolobus acidocaldarius sensitivity to pH changes

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