Phyletic Distribution and Lineage-Specific Domain Architectures of Archaeal Two-Component Signal Transduction Systems

Abstract

The two-component signal transduction (TCS) machinery is a key mechanism of sensing environmental changes in the prokaryotic world. TCS systems have been characterized thoroughly in bacteria but to a much lesser extent in archaea. Here, we provide an updated census of more than 2,000 histidine kinases and response regulators encoded in 218 complete archaeal genomes, as well as unfinished genomes available from metagenomic data. We describe the domain architectures of the archaeal TCS components, including several novel output domains, and discuss the evolution of the archaeal TCS machinery. The distribution of TCS systems in archaea is strongly biased, with high levels of abundance in haloarchaea and thaumarchaea but none detected in the sequenced genomes from the phyla Crenarchaeota, Nanoarchaeota, and Korarchaeota. The archaeal sensor histidine kinases are generally similar to their well-studied bacterial counterparts but are often located in the cytoplasm and carry multiple PAS and/or GAF domains. In contrast, archaeal response regulators differ dramatically from the bacterial ones. Most archaeal genomes do not encode any of the major classes of bacterial response regulators, such as the DNA-binding transcriptional regulators of the OmpR/PhoB, NarL/FixJ, NtrC, AgrA/LytR, and ActR/PrrA families and the response regulators with GGDEF and/or EAL output domains. Instead, archaea encode multiple copies of response regulators containing either the stand-alone receiver (REC) domain or combinations of REC with PAS and/or GAF domains. Therefore, the prevailing mechanism of archaeal TCS signaling appears to be via a variety of protein-protein interactions, rather than direct transcriptional regulation.IMPORTANCE Although the Archaea represent a separate domain of life, their signaling systems have been assumed to be closely similar to the bacterial ones. A study of the domain architectures of the archaeal two-component signal transduction (TCS) machinery revealed an overall similarity of archaeal and bacterial sensory modules but substantial differences in the signal output modules. The prevailing mechanism of archaeal TCS signaling appears to involve various protein-protein interactions rather than direct transcription regulation. The complete list of histidine kinases and response regulators encoded in the analyzed archaeal genomes is available online at http://www.ncbi.nlm.nih.gov/Complete_Genomes/TCSarchaea.html.

Conservation of an Ancient Oxidation Response That Controls Archaeal Epigenetic Traits Through Chromatin Protein Networks

“…However, such proteins are often present in the eukaryotic nucleus and have regulatory effects (49). As archaea are deficient in multi-domain proteins (50) and Crenarchaeota are deficient in two-component regulatory systems (51), these metabolic proteins may have regulatory interactions with chromatin and represent signal transduction pathways. Some archaeal proteins have motifs that appear to be proto-nuclear localization signals (52), which may also explain their presence near the chromosome.…”

Exploring the (Almost) Unknown: Archaeal Two-Component Systems

“…The capacity to sense signals in the extracytoplasmic space was proposed as a major force that has led to the evolution of TCSs from OCSs (1). Several studies have calculated the percentage of bacterial SKs with transmembrane regions, which was found to be between 73 and 88% (1,4,7,8). Most of these proteins are suspected to operate by a mechanism involving extracytoplasmic signal sensing.…”

“…For example, a PubMed search retrieved about 80 times as many publications if the term "two-component system" was combined with "bacteria" than if it was combined with "archaea." In the current issue of Journal of Bacteriology, Galperin and coworkers publish an excellent bioinformatics study in which they have analyzed TCS genes from 218 complete archaeal genomes, as well as from unfinished genomes of metagenomic data sets (7). Like all good scientific articles, the study of Galperin et al prompts many questions, which in turn serve to define experimental strategies to provide the answers.…”

Thiol‐based redox sensing in the methyltransferase associated sensor kinase RdmS in Methanosarcina acetivorans

“…The phosphoryl group is then transferred to a conserved aspartate residue within a receiver domain of the RR. In Archaea, TCS (aTCS) are most abundant in Halobacteria and Methanomicrobia (Galperin et al, 2018). Only very few aTCS have been described in the literature like the temperature-responsive aTCS LtrK/LtrR from Methanococcus burtonii (Najnin et al, 2016), the aTCS FilI/FilRs from Methanosaeta harundinacea (Li et al, 2014) or the chemotaxis aTCS of CheA with CheY and CheB from Halobacterium salinarium .…”

“…Only very few aTCS have been described in the literature like the temperature-responsive aTCS LtrK/LtrR from Methanococcus burtonii (Najnin et al, 2016), the aTCS FilI/FilRs from Methanosaeta harundinacea (Li et al, 2014) or the chemotaxis aTCS of CheA with CheY and CheB from Halobacterium salinarium . Archaeal SK are generally similar to the bacterial ones, commonly possessing PAS and/or GAF domains (Galperin et al, 2018). While most bacterial SK are membrane-bound, those from Archaea are often located in the cytoplasm indicating an important role in perceiving signals inside the cell.…”