Multiparametric Analyses Reveal the pH-Dependence of Silicon Biomineralization in Diatoms

Abstract

Diatoms, the major contributors of the global biogenic silica cycle in modern oceans, account for about 40% of global marine primary productivity. They are an important component of the biological pump in the ocean, and their assemblage can be used as useful climate proxies; it is therefore critical to better understand the changes induced by environmental pH on their physiology, silicification capability and morphology. Here, we show that external pH influences cell growth of the ubiquitous diatom Thalassiosira weissflogii, and modifies intracellular silicic acid and biogenic silica contents per cell. Measurements at the single-cell level reveal that extracellular pH modifications lead to intracellular acidosis. To further understand how variations of the acid-base balance affect silicon metabolism and theca formation, we developed novel imaging techniques to measure the dynamics of valve formation. We demonstrate that the kinetics of valve morphogenesis, at least in the early stages, depends on pH. Analytical modeling results suggest that acidic conditions alter the dynamics of the expansion of the vesicles within which silica polymerization occurs, and probably its internal pH. Morphological analysis of valve patterns reveals that acidification also reduces the dimension of the nanometric pores present on the valves, and concurrently overall valve porosity. Variations in the valve silica network seem to be more correlated to the dynamics and the regulation of the morphogenesis process than the silicon incorporation rate. These multiparametric analyses from single-cell to cell-population levels demonstrate that several higher-level processes are sensitive to the acid-base balance in diatoms, and its regulation is a key factor for the control of pattern formation and silicon metabolism.

Impact of ocean acidification on Arctic phytoplankton blooms and dimethyl sulfide concentration under simulated ice-free and under-ice conditions

“…The former is the most likely explanation since diatom abundance increased in all experimental treatments and numerically dominated the cell community > 2 µm at T5 and T9, irrespective of the pH T level tested. This explanation is also consistent with laboratory studies that previously reported an impairment of Si(OH) 4 uptake in diatom cultures grown at low pH (Milligan et al, 2004;Hervé et al, 2012;Mejía et al, 2013). In Hervé et al (2012), the cells exhibited similar growth rates at high and low pH, implying that the negative impact of a low pH on silification does not preclude bloom development in nature.…”

Photophysiological responses of marine diatoms to elevated CO2 and decreased pH: a review

“…With a further increase of CO 2 concentration in the atmosphere to 800-1000 ppmv under the IPCC A1F1 scenario (Houghton et al 2001), by the end of this century, pH of the surface oceans will decrease by another 0.3-0.4 units Sabine et al 2004;Orr et al 2005), thus, increasing [H + ] by 100-150%. Consequently, organisms in the euphotic zone will be exposed to a higher CO 2 and a lower pH, and their physiologies will respond to changes in seawater carbonate chemistry, as well as to secondary changes in ionic speciation and cell surface chemistry driven by decreasing pH (Millero et al 2009;Flynn et al 2012;Hervé et al 2012;Sugie and Yoshimura 2013). These chemical changes can directly affect physiology of marine organisms (Pörtner and Farrell 2008), but can also indirectly influence organismal responses to other environmental factors including UV radiation (Sobrino et al 2008;Gao et al 2009;Chen and Gao 2011;Li et al 2012a), light (Bartual and Galvez 2002;Sobrino et al 2008;McCarthy et al 2012;Li and Campbell 2013), temperature change (Pörtner and Farrell 2008;Zou et al 2011) or nutrients (Burkhardt and Riebesell 1997;Burkhardt et al 1999;Riebesell and Tortell 2011;Li et al 2012b).…”

Intracellular pH and its response to CO2-driven seawater acidification in symbiotic versus non-symbiotic coral cells

“…The fluorescent dye BCECF-AM, in conjunction with confocal microscopy, has been widely used to study pH i in marine algae (Hervé et al, 2012) as its dual-excitation spectral properties allow fluorescence measurements to be taken that are not compounded by chlorophyll autofluorescence (>640 nm). In this study, confocal microscopy was conducted on a LSM 710 confocal microscope equipped with UV and visible laser lines.…”