Profiling molecular and behavioral circadian rhythms in the non-symbiotic sea anemone Nematostella vectensis

Abstract

Endogenous circadian clocks are poorly understood within early-diverging animal lineages. We have characterized circadian behavioral patterns and identified potential components of the circadian clock in the starlet sea anemone, Nematostella vectensis: a model cnidarian which lacks algal symbionts. Using automatic video tracking we showed that Nematostella exhibits rhythmic circadian locomotor activity, which is persistent in constant dark, shifted or disrupted by external dark/light cues and maintained the same rate at two different temperatures. This activity was inhibited by a casein kinase 1δ/ε inhibitor, suggesting a role for CK1 homologue(s) in Nematostella clock. Using high-throughput sequencing we profiled Nematostella transcriptomes over 48 hours under a light-dark cycle. We identified 180 Nematostella diurnally-oscillated transcripts and compared them with previously established databases of adult and larvae of the symbiotic coral Acropora millepora, revealing both shared homologues and unique rhythmic genes. Taken together, this study further establishes Nematostella as a non-symbiotic model organism to study circadian rhythms and increases our understanding about the fundamental elements of circadian regulation and their evolution within the Metazoa

Transcriptional remodelling upon light removal in a model cnidarian: Losses and gains in gene expression

“…PAR‐bZIPb had a significant period of 28 hr with peak expression in mid‐afternoon (Table , Figure ). The transcription factor helt and the CiPC homolog each had a significant period of 24 hr and were previously identified to have diel expression under LD conditions in cnidarians (Oren et al, ; Shoguchi, Tanaka, Shinzato, Kawashima, & Satoh, ). Consistent with those earlier studies, helt and CiPC expression peaked mid‐morning (ZT = 6) and during subjective night (ZT = 24), respectively ( p ‐value <.01; Table ).…”

“…Nematostella has orthologs (bHLH‐PAS members Clock and Cycle/Bmal ) or homologs (cryptochromes, PAR‐bZIP) to genes centrally involved in the bilaterian circadian clock, many of which have oscillating expression under light:dark conditions (Reitzel et al, , ). In addition, hundreds of genes show differential expression under diel lighting (Leach, Macrander, Peres, & Reitzel, ; Oren et al, ), but many of these have no evidence for differential expression when animals are cultured under extended periods of darkness (Leach et al, ; Peres et al, ). Together, these previous studies have shown this species has a diverse transcriptional response to light but the maintenance of these oscillations in gene expression is largely unknown, except after long periods of time (>20 days; Leach et al, ; Peres et al, ; Reitzel et al, ; Reitzel et al, ).…”

Diel patterning in the bacterial community associated with the sea anemone Nematostella vectensis

“…By assessing bacterial abundance across diel and constant conditions, our research sheds light on the potential of microbial interactions in the regulation of host anemone cyclic behavior and physiology measured in other studies (Hendricks et al, 2012;Maas et al, 2016;Oren et al, 2015). By assessing bacterial abundance across diel and constant conditions, our research sheds light on the potential of microbial interactions in the regulation of host anemone cyclic behavior and physiology measured in other studies (Hendricks et al, 2012;Maas et al, 2016;Oren et al, 2015).…”

“…Further, how much of the holobiont rhythmicity is due to a direct response to environmental cues (e.g., light) or is driven by endogenous mechanisms remains an active area of research (Brady, Willis, Harder, & Vize, 2016;Leach, Macrander, Peres, & Reitzel, 2018;Oren et al, 2015;Vize, 2009). Further, how much of the holobiont rhythmicity is due to a direct response to environmental cues (e.g., light) or is driven by endogenous mechanisms remains an active area of research (Brady, Willis, Harder, & Vize, 2016;Leach, Macrander, Peres, & Reitzel, 2018;Oren et al, 2015;Vize, 2009).…”

“…Similar to corals, N. vectensis exhibits nocturnal patterns in behavior [e.g., circadian locomotion and body expansion (Hendricks, Byrum, & Meyer-Bernstein, 2012;Oren et al, 2015)], gene expression [e.g., immunity and stress tolerance (Leach et al, 2018)], and metabolism (Maas, Jones, Reitzel, & Tarrant, 2016). Similar to corals, N. vectensis exhibits nocturnal patterns in behavior [e.g., circadian locomotion and body expansion (Hendricks, Byrum, & Meyer-Bernstein, 2012;Oren et al, 2015)], gene expression [e.g., immunity and stress tolerance (Leach et al, 2018)], and metabolism (Maas, Jones, Reitzel, & Tarrant, 2016).…”