Effect of CO2-induced seawater acidification on growth, photosynthesis and inorganic carbon acquisition of the harmful bloom-forming marine microalga, Karenia mikimotoi.

Shunxin Hu,You Wang,Bin Zhou,Ying Wang,Yan Zhao,Xinyu Zhao,Xinxin Zhang,Xuexi Tang

doi:10.1371/journal.pone.0183289

Abstract

Karenia mikimotoi is a widespread, toxic and non-calcifying dinoflagellate, which can release and produce ichthyotoxins and hemolytic toxins affecting the food web within the area of its bloom. Shifts in the physiological characteristics of K. mikimotoi due to CO2-induced seawater acidification could alter the occurrence, severity and impacts of harmful algal blooms (HABs). Here, we investigated the effects of elevated pCO2 on the physiology of K. mikimotoi. Using semi-continuous cultures under controlled laboratory conditions, growth, photosynthesis and inorganic carbon acquisition were determined over 4–6 week incubations at ambient (390ppmv) and elevated pCO2 levels (1000 ppmv and 2000 ppmv). pH-drift and inhibitor-experiments suggested that K. mikimotoi was capable of acquiring HCO3-, and that the utilization of HCO3- was predominantly mediated by anion-exchange proteins, but that HCO3- dehydration catalyzed by external carbonic anhydrase (CAext) only played a minor role in K. mikimotoi. Even though down-regulated CO2 concentrating mechanisms (CCMs) and enhanced gross photosynthetic O2 evolution were observed under 1000 ppmv CO2 conditions, the saved energy did not stimulate growth of K. mikimotoi under 1000 ppmv CO2, probably due to the increased dark respiration. However, significantly higher growth and photosynthesis [in terms of photosynthetic oxygen evolution, effective quantum Yield (Yield), photosynthetic efficiency (α), light saturation point (Ek) and ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) activity] were observed under 2000 ppmv CO2 conditions. Furthermore, elevated pCO2 increased the photo-inhibition rate of photosystem II (β) and non-photochemical quenching (NPQ) at high light. We suggest that the energy saved through the down-regulation of CCMs might lead to the additional light stress and photo-damage. Therefore, the response of this species to elevated CO2 conditions will be determined by more than regulation and efficiency of CCMs.

Highlights

Ocean acidification refers to the ongoing reduction in the ocean pH over an extended period of time, which is primarily caused by the uptake of anthropogenic CO2 from the atmosphere [1, 2]
We evaluated growth, photosynthesis, dark respiration and the concentrating mechanisms (CCMs) modes of K. mikimotoi exposed to three different pCO2 levels: 390 ppmv which is the present pH value, as well as 1000 ppmv and pCO2: 2000 ppmv, which are predicted to be possible conditions in 2100 and 2300, respectively
The dissolved inorganic carbon (DIC), CO2 and HCO3- concentrations in the 1000 ppmv-treated system were increased by 7.0%, 125.9% and 10.1%, respectively, whereas in the 2000 ppmv-treated system, these values increased by 12.1%, 361.4% and 15.5%, respectively

Summary

Introduction

Ocean acidification refers to the ongoing reduction in the ocean pH over an extended period of time, which is primarily caused by the uptake of anthropogenic CO2 from the atmosphere [1, 2]. The other is that, increased pCO2 could down-regulate the energetically costly operation of CCMs. Many marine phytoplankton species down-regulate their operation of CCMs at high pCO2 conditions, as revealed by a lower photosynthetic affinity for CO2, decreased activities of carbonic anhydrase and/or a lower contribution of HCO3-assimilation [9,10,11,12]. Many marine phytoplankton species down-regulate their operation of CCMs at high pCO2 conditions, as revealed by a lower photosynthetic affinity for CO2, decreased activities of carbonic anhydrase and/or a lower contribution of HCO3-assimilation [9,10,11,12] This is taken as evidence that elevated pCO2 exerts positive effects on the growth and photosynthesis of species bearing CCMs[9, 13,14,15]. We hypothesized that (1) the operation of CCMs will be down-regulated with elevated pCO2 and (2) the reduction in the energy costs of CCMs will benefit growth and photosynthesis of K. mikimotoi

Materials and methods

Results

Discussion