Assessment of the independent and combined effects of copper and polycyclic aromatic hydrocarbons on gametogenesis and sporophyte development of the kelp Lessonia spicata (Phaeophyceae, Ochrophyta)

Camila Espinoza-González,Jorge Rivas,Alejandra Núñez,Andrés Meynard,Nicolás Latorre-Padilla,Carolina Oyarzo-Miranda,Loretto Contreras-Porcia,Francisco Castañeda

doi:10.1007/s10811-021-02552-7

Camila Espinoza-González, Jorge Rivas + Show 6 more

Open Access

https://doi.org/10.1007/s10811-021-02552-7

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Abstract

Coastal shores near the industrial park of Quintero Bay in central Chile exhibit increasing concentrations of copper (Cu) and polycyclic aromatic hydrocarbons (PAHs), well above international standards. This raises concern about their combined toxic effects on early development stages of kelps. Accordingly, we aimed to assess more accurately the independent and combined effects of Cu and PAHs on gametogenesis and sporophyte development in the kelp Lessonia spicata from central Chile by in vitro cultivation. Independent Cu and PAH trials were performed using increasing nominal concentrations of Cu and PAHs in the ranges 0.8–200 µg L−1 and 0.05–100 µg L−1, respectively. Cu and PAH median effective concentrations (EC50) on gametogenesis and early sporophyte formation were calculated using DRC in the R environment. Then, combined EC50 Cu + PAH trials were conducted to determine their effects on gametogenesis and sporophyte formation. Cu EC50 values on gametogenesis and sporophyte formation were up to three orders of magnitude lower than EC50 reported previously on spore germination in kelps. The gametogenesis (EC50 = 1.39 µg L−1) was more sensitive to Cu than sporophyte formation (EC50 = 11 µg L−1). Inversely, sporophyte formation (EC50 = 0.04 µg L−1) was more sensitive to PAHs (EC50 = 0.11 µg L−1). Considering the entire exposure period, the combined EC50 Cu + PAH exposure was the most harmful and rapid for L. spicata microscopic stages, especially the synergistic effect on early sporophytes. This highlights the need to acquire an integrated knowledge of the seasonal variation of pollutants and their combination on highly intervened coasts.

Highlights

Heavy metals (HMs) and polycyclic aromatic hydrocarbons (PAHs) are ubiquitous contaminants and are highly toxic and persistent in coastal environments
Our results show that in L. spicata, gametogenesis is the development stage most affected by Cu toxicity, whereas PAH toxicity exerted a higher impact on sporophytes formation
The most harmful effect on the early development of L. spicata was the toxic exposure to the combined EC50 Cu + PAHs, which manifested high negative effects faster and earlier than the independent Cu or PAH treatments

Summary

Introduction

Heavy metals (HMs) and polycyclic aromatic hydrocarbons (PAHs) are ubiquitous contaminants and are highly toxic and persistent in coastal environments. Toxic PAHs exposure induces early developmental alterations, reduction in growth, photosynthesis inhibition, reduction in chlorophyll content, deregulation of cellular homeostasis, oxidative stress, cell death, upregulation of antioxidant systems, and mutagenic and carcinogenic effects (e.g., Jajoo et al 2014; Ewa and Danuta 2017; Hernández-Vega et al 2017). Copper (Cu) is required for the normal growth and development of photosynthetic organisms, which have evolved protein Cu transporters in the plasma and organelles membranes (i.e., Cu transporter family and the group B transport family P1B-type ATPases) regulating its homeostasis in accordance with concentration levels in the environment (Blaby-Haas and Merchant, 2012; Contreras-Porcia et al 2017). Despite its requirement as a micronutrient, above a certain threshold concentration, Cu inhibits early development and several physiological processes, such as photosynthetic electron transport, mitochondrial respiration, cell wall metabolism, oxidative stress response, and hormone signaling (Kumar et al 2021)

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