Rhythms of Gene Expression in a Fluctuating Intertidal Environment

Abstract

The physiological strategies that enable organisms to thrive in habitats where environmental factors vary dramatically on a daily basis are poorly understood. One of the most variable and unpredictable habitats on earth is the marine rocky intertidal zone located at the boundary between the terrestrial and marine environments. Mussels dominate rocky intertidal habitats throughout the world and, being sessile, endure wide variations in temperature, salinity, oxygen, and food availability due to diurnal, tidal, and climatic cycles. Analysis of gene-expression changes in the California ribbed mussel (Mytilus californianus) at different phases in the tidal cycle reveals that intertidal mussels exist in at least four distinct physiological states, corresponding to a metabolism and respiration phase, a cell-division phase, and two stress-response signatures linked to moderate and severe heat-stress events. The metabolism and cell-division phases appear to be functionally linked and are anticorrelated in time. The magnitudes and timings of these states varied by vertical position on the shore and appear to be driven by microhabitat conditions. The results provide new insights into the strategies that allow life to flourish in fluctuating environments and demonstrate the importance of time course data collected from field animals in situ in understanding organism-environment interactions.

The role of stochastic thermal environments in modulating the thermal physiology of an intertidal limpet, Lottia digitalis

“…Intertidal animals tailor their cellular stress response mechanisms to be quickly initiated following the onset of high tide such that recovery is complete before the start of the next low tide period (Hofmann and Somero, 1996;Tomanek and Somero, 2000;Schill et al, 2002;Clark et al, 2008;Zhang et al, 2014). Transcriptomics of Mytilus californianus have also shown upregulated gene expression of recovery mechanisms, including antioxidants, to return to cellular homeostasis during the high tide period before the next low tide period (Gracey et al, 2008;Place et al, 2012). It may have been that the periods of immersion during high tide were sufficient to mitigate any acquired stress during the daytime low tide periods of the acclimation treatments by available antioxidants.…”

“…Although cellular stress response mechanisms to heat stress have been extensively studied in intertidal organisms (Hofmann and Somero, 1995;Roberts et al, 1997;Sokolova and Pörtner, 2001;Todgham et al, 2005;Gardeström et al, 2007;Dong et al, 2008a,b;Han et al, 2013;Zhang et al, 2014), only a few studies have considered the mechanistic strategies under unpredictable heating conditions associated with natural tidal cycles (Gracey et al, 2008;Connor and Gracey, 2011). Stress response mechanisms are energetically costly and require animals to increase metabolic rates (Sokolova et al, 2012).…”

“…We predicted that L. digitalis acclimated to stochastic tidal regimes would be less sensitive and have a higher tolerance to heat stress than limpets exposed to predictable temperatures. The variability in the magnitude of temperature increase during periods of emersion would prime the limpets to maintain protective mechanisms when exposed to the highest temperatures; however, emersion periods with low to moderate increases in temperature would provide limpets with reprieve from consistently high low-tide temperatures, which could minimize accumulated damage from heat stress and improve efficiency in the recruiting of protective mechanisms (Hofmann and Somero, 1996;Gracey et al, 2008;Denny et al, 2011;Zhang et al, 2014;Huang et al, 2015).…”

Spatiotemporal compartmentalization of key physiological processes during muscle precursor differentiation

“…Spatiotemporal compartmentalization of metabolic processes has been reported in various organisms, ranging from cyanobacteria and yeast to animals (24)(25)(26). In vertebrates, functions, such as the cell cycle or energy production, are also under temporal circadian regulation and are differentially regulated depending on the organ considered (27).…”

Triggers of the HSP70 stress response: environmental responses and laboratory manipulation in an Antarctic marine invertebrate (Nacella concinna)

“…The inducible HSP70 is often described as one of the major responses to acute heat stress even when 1,000s of genes are surveyed in microarrays (cf. Gracey et al 2008); however, the constitutive HSC70 has been designated the main heat-dependant HSP70 family member in the Pacific white shrimp (Litopenaeus vannamei; Wu et al 2008). This latter example may be species specific as there is increasing evidence that although HSC70 may upregulated by acute heat stress, it is often more likely to correlate with longer-term chronic stress such as that described here, in fluctuating temperature regimes (Podrabsky and Somero 2004;Todgham et al 2006) and under environmentally diverse bio-geographical distributions (Fangue et al 2006;Place et al 2008).…”