Combined effects of seawater acidification and benzo(a)pyrene on the physiological performance of the marine bloom-forming diatom Skeletonema costatum

Highlights

• Skeletonema costatum was tolerant to low and moderate benzo(a)pyrene concentrations.

• The high benzo(a)pyrene concentration remarkably inhibited growth and photosynthesis.

• Negative effects of ocean acidification were detected at the high benzo(a)pyrene level.

Abstract

The combined effects of polycyclic aromatic hydrocarbons and seawater acidification are poorly understood. Hence, we exposed the bloom-forming diatom Skeletonema costatum to four concentrations (0, 0.1, 1 and 10 μg L⁻¹) of benzo(a)pyrene and two pCO₂ levels (400 and 1000 μatm) to investigate its physiological performance. The growth and photosynthesis of S. costatum were tolerant to low and moderate benzo(a)pyrene concentrations regardless of the pCO₂ level. However, the highest benzo(a)pyrene concentration had remarkably adverse effects on most parameters, decreasing the growth rate by 69%. Seawater acidification increased the sensitivity to high light stress, as shown by the lower maximum relative electron transport rate and light saturation point at the highest benzo(a)pyrene concentration. Our results suggested that benzo(a)pyrene could be detrimental to diatoms at a habitat-relevant level, and seawater acidification might further decrease its light tolerance, which would have important ramifications for the community structure and primary production in coastal waters.

Introduction

Polycyclic aromatic hydrocarbons (PAHs) are generally mutagenic, teratogenic, and carcinogenic (Lehr and Jerina, 1977). They are listed as priority pollutants due to their toxicity and impacts on organisms including human beings. PAHs are mainly produced by anthropogenic activities, such as the incomplete combustion of carbonaceous materials and leakage of coal tar, asphalt, and virous industrial mineral oils. PAHs in marine environments are mainly caused by petroleum discharge, atmospheric deposition, and land-sourced pollution (Howsam and Jones, 1998). The concentrations of total PAHs in coastal waters could reach ~30 μg L⁻¹ (Zhou and Maskaoui, 2003), which is suggested to be detrimental to pico- and nanophytoplankton cells (Carvalho and Lettieri, 2011; Kottuparambil and Agusti, 2018). It has been suggested that PAHs inhibit photosynthesis, respiration, and electron transport system (Singh and Gaur, 1988), reduce DNA synthesis (Cerezo and Agusti, 2015), and increase oxidative stress in phytoplankton (Vega-López et al., 2013). Benzo(a)pyrene is a five-ring PAH, that has been chosen frequently as a representative PAH to investigate its impacts. The concentration of benzo(a)pyrene in coastal waters has been recorded as high as 5 μg L⁻¹ (Zhou and Maskaoui, 2003).

Another environmental change caused by anthropogenic activities is the increasing atmospheric CO₂. The ocean absorbs about 30% of the CO₂ emitted by humans (Sabine et al., 2004), and carbonic acid is generated by the reaction of CO₂ and seawater. The dissolution of atmospheric CO₂ and dissociation of carbonic acid lead to three main forms of inorganic carbon in seawater: dissolved CO₂, bicarbonate, and carbonate (Zeebe and Wolf-Gladrow, 2001). At the current ocean pH level, the main form of seawater inorganic carbon is bicarbonate (˃ 85%) (Zeebe, 2012). Rising atmospheric CO₂ concentrations cause the decrease of seawater pH, carbonate concentration, and calcium carbonate saturation, while the concentrations of dissolved CO₂ and bicarbonate ion in seawater increase, which is termed as ocean acidification (Doney et al., 2009). The pH value of ocean surface water has fallen by 0.1 units since the Industrial Revolution (Orr et al., 2005; Doney, 2010), which is the fastest rate of decrease in the last 20 million years (Turley et al., 2006). At this rate, the pH of the surface seawater will drop by 0.3–0.4 units by the end of this century (Gattuso et al., 2015).

The influences of ocean acidification on the base of the marine food web, phytoplankton, have attracted much attention. Diatoms, as a key phytoplankton group, contribute about a quarter of the global primary productivity (Falkowski et al., 2004). The responses of diatoms to ocean acidification would alter the amount of photosynthetic carbon sequestration and the export of organic matter to the deep sea to a remarkable degree. Various studies have concluded that ocean acidification would either promote or do not affect the growth and photosynthesis of diatoms based on short-term simulation experiments. However, under the existence of other stressors, the lowered pH could significantly inhibit the physiological performance of diatoms (Gao et al., 2012; Li and Campbell, 2013; Passow and Laws, 2015; Li et al., 2021). For instance, the photosynthetic rate of a diatom Thalassiosira pseudonana was inhibited by elevated pCO₂ during nitrogen limitation (Hennon et al., 2014), while it remained unaffected during nitrogen replete conditions (Li et al., 2018).

An increasing number of studies have focused on the interactive effects of environmental factors given the complex conditions in the ocean. However, there is limited knowledge on the combined influences of PAHs and seawater acidification on phytoplankton, which would hinder the overall understanding of the effects of PAHs in the oceans in the future. The aim of the present study was to investigate the combined effects of benzo(a)pyrene, a typical and ubiquitous PAH, and seawater acidification on the physiological performance of the bloom-forming diatom Skeletonema costatum.