Abstract
Organisms often employ ecophysiological strategies to exploit environmental conditions and ensure bio-energetic success. However, the many complexities involved in the differential expression and flexibility of these strategies are rarely fully understood. Therefore, for the first time, using a three-part cross-disciplinary laboratory experimental analysis, we investigated the diversity and plasticity of photoresponsive traits employed by one family of environmentally contrasting, ecologically important phytoflagellates. The results demonstrated an extensive inter-species phenotypic diversity of behavioural, physiological, and compositional photoresponse across the Chlamydomonadaceae, and a multifaceted intra-species phenotypic plasticity, involving a broad range of beneficial photoacclimation strategies, often attributable to environmental predisposition and phylogenetic differentiation. Deceptively diverse and sophisticated strong (population and individual cell) behavioural photoresponses were observed, with divergence from a general preference for low light (and flexibility) dictated by intra-familial differences in typical habitat (salinity and trophy) and phylogeny. Notably, contrasting lower, narrow, and flexible compared with higher, broad, and stable preferences were observed in freshwater vs. brackish and marine species. Complex diversity and plasticity in physiological and compositional photoresponses were also discovered. Metabolic characteristics (such as growth rates, respiratory costs and photosynthetic capacity, efficiency, compensation and saturation points) varied elaborately with species, typical habitat (often varying more in eutrophic species, such as Chlamydomonas reinhardtii), and culture irradiance (adjusting to optimise energy acquisition and suggesting some propensity for low light). Considerable variations in intracellular pigment and biochemical composition were also recorded. Photosynthetic and accessory pigments (such as chlorophyll a, xanthophyll-cycle components, chlorophyll a:b and chlorophyll a:carotenoid ratios, fatty acid content and saturation ratios) varied with phylogeny and typical habitat (to attune photosystem ratios in different trophic conditions and to optimise shade adaptation, photoprotection, and thylakoid architecture, particularly in freshwater environments), and changed with irradiance (as reaction and harvesting centres adjusted to modulate absorption and quantum yield). The complex, concomitant nature of the results also advocated an integrative approach in future investigations. Overall, these nuanced, diverse, and flexible photoresponsive traits will greatly contribute to the functional ecology of these organisms, addressing environmental heterogeneity and potentially shaping individual fitness, spatial and temporal distribution, prevalence, and ecosystem dynamics.
Highlights
Organisms often employ numerous and varied ecophysiological strategies to exploit environmental conditions and ensure ecological success (e.g., Grémillet et al, 2005; Clegg et al, 2012)
LL and HL cultures of the marine and brackish species displayed a preference for higher light, 47–182 μmol photons m−2 s−1 (Ftest, P < 0.001: Tukey test P < 0.05), significantly greater than the preferences of all freshwater LL and both LL and HL cultures of C. chlorastera, C. moewusii, and C. reinhardtii
We recorded a wide array of photoresponsive traits across the Chlamydomonadaceae, and an ecophysiological diversity and plasticity that may be phylogenetically derived and attributable to the different typical habitats of species
Summary
Organisms often employ numerous and varied ecophysiological strategies to exploit environmental conditions and ensure ecological success (e.g., Grémillet et al, 2005; Clegg et al, 2012). Such diversity and “phenotypic plasticity” (rapid, reversible adjustment of an organism’s observable traits) can maximise ecological fitness in fluctuating environments (e.g., West-Eberhard, 1989). Phytoflagellates are an ecologically important group of eukaryotic microorganisms whose dual motility and photosynthesis bridge the divide between animal and plant ecophysiology They are integral and thrive in a wide range of habitats; and they have recently assumed increased relevance due to their role in harmful algal blooms and biofuel synthesis (e.g., Smayda, 1997; Benning, 2015). Widely used in biomolecular investigations (e.g., Merchant et al, 2007), their ecology still remains uncertain, and the ecophysiological predisposition and differentiation of environmentally contrasting species have rarely been described
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