Distinct physiological responses ofCoccolithus braarudiilife cycle phases to light intensity and nutrient availability

Abstract

Coccolithophores feature a haplo-diplontic life cycle comprised of diploid cells producing heterococcoliths and haploid cells producing morphologically different holococcoliths. These life cycle phases of each species appear to have distinct spatial and temporal distributions in the oceans, with the heavily-calcified heterococcolithophores (HET) often more prevalent in winter and at greater depths, whilst the lightly-calcified holococcolithophores (HOL) are more abundant in summer and in shallower waters. The haplo-diplontic life cycle may therefore allow coccolithophores to expand their ecological niche, switching between life cycle phases to exploit conditions that are more favourable. However, coccolithophore life cycles remain poorly understood and fundamental information on the physiological differences between life cycle phases is required if we are to better understand the ecophysiology of coccolithophores. In this study, we have examined the physiology of HET and HOL phases of the coccolithophore Coccolithus braarudii in response to changes in light and nutrient availability. We found that the HOL phase was more tolerant to high light than the HET phase, which exhibited defects in calcification at high irradiances. The HET phase exhibited defects in coccolith formation under both nitrate (N) and phosphate (P) limitation, whilst no defects in calcification were detected in the HOL phase. The HOL phase grew to a higher cell density under P-limitation than N-limitation, whereas no difference was observed in the maximum cell density reached by the HET phase at these nutrient concentrations. HET cells grown under a light:dark cycle divided primarily in the dark and early part of the light phase, whereas HOL cells continued to divide throughout the 24 h period. The physiological differences may contribute to the distinct biogeographical distributions observed between life cycle phases, with the HOL phase potentially better adapted to high light, low nutrient regimes, such as those found in seasonally stratified surface waters. Highlights: Coccolithus braarudii life cycle phases exhibit different physiological responses. The heavily-calcified heterococcolithophores (HET) life cycle phase is more sensitive to high light. The lightly-calcified holococcolithophores (HOL) life cycle phase may be better suited to growth under low phosphate availability..

Evolutionary Rates in the Haptophyta: Exploring Molecular and Phenotypic Diversity

“…Culture experiments have supported this hypothesis, where two heavily calcified coccolithophore species (Calcidiscus leptoporus and Coccolithus braarudii) increased growth under turbulent, nutrient-rich conditions [138]. Additionally, recent evidence suggests that the HOL phase of C. braarudii is more tolerant to high irradiance as well as phosphate limitation compared to its HET phase [140]. The non-motile, calcified diploid phase of E. huxleyi is commonly found in stratified surface waters, where it is known to form extensive blooms following nutrient depletion by other phytoplankton groups [158,159], whereas its non-calcified, biflagellate cells become progressively more abundant during late-stage bloom periods [160].…”

“…Uptake of organic molecules through osmotrophy has been observed in diploid Ochrosphaera neopolitana, diploid Cruciplacolithus neohelis, and haploid G. oceanica [139] (Figure 8). In addition, diploid C. braarudii was found to survive over extended periods while exposed to darkness, suggesting an alternate mode of energy acquisition [140]. Particle/prey ingestion in these instances was generally low, and likely does not represent a major proportion of energy consumption except in limited taxa, such as the polar coccolithophore family Papposphaeraceae, which lack chloroplasts, or the deep photic zone (DPZ) dwelling Florisphaera profunda and Gladiolithus spp.…”

A critical trade-off between nitrogen quota and growth allows Coccolithus braarudii life cycle phases’ to exploit varying environment

“…The distribution of Coccolithus braarudii varies in the ocean with C. braarudii HET dominating high-nutrient and turbulent regions, while C. braarudii HOL is primarily found in lower-nutrient and more stratified regions (Malinverno et al, 2009;D'Amario et al, 2017). While some previous work suggests that differential response to turbulence (Houdan et al, 2004) and light (Langer et al, 2022) could drive this distribution difference, open questions remain about how physiology differs between the two life cycle phases.…”

“…The life cycle phases of Coccolithus braarudii are morphologically distinct, with the haploid life cycle phase utilizing a holococcolith (HOL) morphology and the diploid life cycle phase utilizing a heterococcolith (HET) morphology (Houdan et al, 2004). Most lab work on C. braarudii has focused on the HET phase, with research on the HOL life cycle phase much more limited (Houdan et al, 2006;Langer et al, 2022).…”

“…Nutrient quota influences nutrient requirement (Litchman et al, 2007) and storage (Falkowski and Oliver, 2007 ;Grover, 1991). Photosynthetic response influences light optima and has previously been suggested to be a key driver in Coccolithus braarudii life cycle distribution (Langer et al, 2022). We also investigated differences in temperature optima, as this is a major driver of coccolithophore life cycle phases in situ (de Vries et al, 2021).…”