Diurnally Entrained Anticipatory Behavior in Archaea

Whitehead, Kenia; Pan, Min; Masumura, Ken-ichi; Bonneau, Richard; Baliga, Nitin S.

doi:10.1371/journal.pone.0005485

Cited by 55 publications

(61 citation statements)

References 53 publications

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“…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%

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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%

“…Among archaea, diurnal gene expression has been demonstrated only in Halobacteria (24,57,60). It has been shown that KaiC-like proteins undergo cyclic expression, and deletion of most of them affected the expression of the others, suggesting that Halobacteria indeed might have a bona fide KaiC-based circadian mechanism (38).…”

Section: Resultsmentioning

confidence: 99%

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

Makarova

Galperin

Koonin

2017

mBio

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“…Disproving this notion, Huang et al (1990) demonstrated that the phototrophic marine cyanobacterium Synechococcus elongatus displays a robust circadian rhythm. More recently, it was shown that photoheterotrophic Halobacterium synchronize their physiologies with a light-dark cycle (Whitehead et al, 2009). Evidence of this diel behavior has been found in individual organisms throughout the microbial world, pointing to its critical role in the ecology and evolution of microbial communities.…”

Section: Discussionmentioning

confidence: 99%

Metagenomic and lipid analyses reveal a diel cycle in a hypersaline microbial ecosystem

et al. 2015

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Marine microbial communities experience daily fluctuations in light and temperature that can have important ramifications for carbon and nutrient cycling. Elucidation of such short time scale community-wide dynamics is hindered by system complexity. Hypersaline aquatic environments have lower species richness than marine environments and can be well-defined spatially, hence they provide a model system for diel cycle analysis. We conducted a 3-day time series experiment in a well-defined pool in hypersaline Lake Tyrrell, Australia. Microbial communities were tracked by combining cultivation-independent lipidomic, metagenomic and microscopy methods. The ratio of total bacterial to archaeal core lipids in the planktonic community increased by up to 58% during daylight hours and decreased by up to 32% overnight. However, total organism abundances remained relatively consistent over 3 days. Metagenomic analysis of the planktonic community composition, resolved at the genome level, showed dominance by Haloquadratum species and six uncultured members of the Halobacteriaceae. The post 0.8 μm filtrate contained six different nanohaloarchaeal types, three of which have not been identified previously, and cryo-transmission electron microscopy imaging confirmed the presence of small cells. Notably, these nano-sized archaea showed a strong diel cycle, with a pronounced increase in relative abundance over the night periods. We detected no eukaryotic algae or other photosynthetic primary producers, suggesting that carbon resources may derive from patchily distributed microbial mats at the sediment-water interface or from surrounding land. Results show the operation of a strong community-level diel cycle, probably driven by interconnected temperature, light abundance, dissolved oxygen concentration and nutrient flux effects.

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“…Specifically, the expression of ϳ12% of genes from the halophilic archaeon Halobacterium salinarum NRC-1 has been found to oscillate with either ultradian (13-h) or circadian (22-h) periodicity under constant conditions after 3 days of entrainment in an LD cycle (98). The halophilic archaeon Haloferax volcanii harbors 4 cryptic kaiC-like genes, cirA, cirB, cirC, and cirD, that share 28% to 33% identity with and 48% to 55% similarity to KaiC from S. elongatus and possess predicted Walker A and B motifs (99).…”

Section: Archaeal Rhythmsmentioning

confidence: 99%

Circadian Rhythms in Cyanobacteria

Cohen

Golden

2015

Microbiol Mol Biol Rev

238

224

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SUMMARYLife on earth is subject to daily and predictable fluctuations in light intensity, temperature, and humidity created by rotation of the earth. Circadian rhythms, generated by a circadian clock, control temporal programs of cellular physiology to facilitate adaptation to daily environmental changes. Circadian rhythms are nearly ubiquitous and are found in both prokaryotic and eukaryotic organisms. Here we introduce the molecular mechanism of the circadian clock in the model cyanobacteriumSynechococcus elongatusPCC 7942. We review the current understanding of the cyanobacterial clock, emphasizing recent work that has generated a more comprehensive understanding of how the circadian oscillator becomes synchronized with the external environment and how information from the oscillator is transmitted to generate rhythms of biological activity. These results have changed how we think about the clock, shifting away from a linear model to one in which the clock is viewed as an interactive network of multifunctional components that are integrated into the context of the cell in order to pace and reset the oscillator. We conclude with a discussion of how this basic timekeeping mechanism differs in other cyanobacterial species and how information gleaned from work in cyanobacteria can be translated to understanding rhythmic phenomena in other prokaryotic systems.

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Diurnally Entrained Anticipatory Behavior in Archaea

Cited by 55 publications

References 53 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

Metagenomic and lipid analyses reveal a diel cycle in a hypersaline microbial ecosystem

Circadian Rhythms in Cyanobacteria

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