Setting the pace: host rhythmic behaviour and gene expression patterns in the facultatively symbiotic cnidarian Aiptasia are determined largely by Symbiodinium

Abstract

BackgroundAll organisms employ biological clocks to anticipate physical changes in the environment; however, the integration of biological clocks in symbiotic systems has received limited attention. In corals, the interpretation of rhythmic behaviours is complicated by the daily oscillations in tissue oxygen tension resulting from the photosynthetic and respiratory activities of the associated algal endosymbiont Symbiodinium. In order to better understand the integration of biological clocks in cnidarian hosts of Symbiodinium, daily rhythms of behaviour and gene expression were studied in symbiotic and aposymbiotic morphs of the sea-anemone Aiptasia diaphana.ResultsThe results showed that whereas circatidal (approx. 12-h) cycles of activity and gene expression predominated in aposymbiotic morphs, circadian (approx. 24-h) patterns were the more common in symbiotic morphs, where the expression of a significant number of genes shifted from a 12- to 24-h rhythm. The behavioural experiments on symbiotic A. diaphana displayed diel (24-h) rhythmicity in body and tentacle contraction under the light/dark cycles, whereas aposymbiotic morphs showed approximately 12-h (circatidal) rhythmicity. Reinfection experiments represent an important step in understanding the hierarchy of endogenous clocks in symbiotic associations, where the aposymbiotic Aiptasia morphs returned to a 24-h behavioural rhythm after repopulation with algae.ConclusionWhilst some modification of host metabolism is to be expected, the extent to which the presence of the algae modified host endogenous behavioural and transcriptional rhythms implies that it is the symbionts that influence the pace. Our results clearly demonstrate the importance of the endosymbiotic algae in determining the timing and the duration of the extension and contraction of the body and tentacles and temporal gene expression.Electronic supplementary materialThe online version of this article (10.1186/s40168-018-0465-9) contains supplementary material, which is available to authorized users.

Symbiotic lifestyle triggers drastic changes in the gene expression of the algal endosymbiont Breviolum minutum (Symbiodiniaceae)

“…The comparative ΔΔ CT s method was used, and fold changes were calculated using the 2 −ΔΔ Ct formula to estimate the relative difference in the number of transcripts between the aposymbiotic and symbiotic samples. Four potential house‐keeping genes were tested: 28S ribosomal RNA gene (Rodriguez‐Lanetty, Phillips, & Weis, ), beta‐actin (Rodriguez‐Lanetty et al, ), 40S ribosomal protein S7 (Lehnert et al, ), and encoding ribosomal protein L11 (RPL11; Sorek et al, ). Samples were normalized to the latter, which was the best performing one and showed the most stable expression pattern across all samples.…”

“…ΔΔCTs method was used, and fold changes were calculated using the 2 −ΔΔCt formula to estimate the relative difference in the number of transcripts between the aposymbiotic and symbiotic samples. Sorek et al, 2018). Samples were normalized to the latter, which was the best performing one and showed the most stable expression pattern across all samples.…”

12h-clock control of central dogma information flow by XBP1s

“…We originally hypothesized that the mammalian 12h clock evolved from the circatidal clock of coastal and estuarine animals that modulate their behavior in tune to the ~12.4 hour ebb and flow of the tides Zhu et al, 2017), which were also established independently from the circadian clock (III et al, 2008;Naylor, 1996;Takekata et al, 2012;Takekata et al, 2014;Zhang et al, 2013). To seek further support for our hypothesis, we analyzed two recently published time series RNA-Seq dataset of two marine animals harboring circatidal clock, aposymbiotic sea anemone Aiptasia diaphaha (Sorek et al, 2018) and the limpet Cellana rota . In both cases, we found large overlap of 12h-cycling transcritptome between mouse and these two species ( Figures 7A-C, S7A-C, Table S12).…”

“…Consensus XBP1s binding motifs located at each gene promoter are also shown. (Q) RNA-Seq data for representative genes in (Sorek et al, 2018) and mouse liver, with both raw data and superimposed ~12h rhythms shown for the mouse liver data. (B) Predicted interactive network construction of these conserved 12h-cycling genes using STRING (Szklarczyk et al, 2015).…”

“…Data are graphed as the box and whisker plot (min to max) in I and mean ± SEM in Q. (Sorek et al, 2018) and mouse liver, with both raw data and superimposed ~12h rhythms shown for the mouse liver data. (B) Predicted interactive network construction of these conserved 12h-cycling genes using STRING (Szklarczyk et al, 2015).…”