Intraspecific variability in membrane proteome, cell growth, and morphometry of the invasive marine neurotoxic dinoflagellate Alexandrium pacificum grown in metal-contaminated conditions

Type Article
Date 2020-05
Language English
Author(s) Chetouhi Cherif1, Masseret Estelle2, Satta Cecilia Teodora3, Balliau Thierry4, Laabir Mohamed2, Jean Natacha1
Affiliation(s) 1 : Mediterranean Institute of Oceanography, Equipe Microbiologie Environnementale et Biotechnologie, UM 110 CNRS/IRD Aix-Marseille Université, Université de Toulon, CS 60584, 83 041 Toulon Cedex 9, France
2 : Marbec, University of Montpellier, IRD, Ifremer, CNRS, 34 095 Montpellier Cedex 5, France
3 : University of Sassari, via Piandanna 4, Agenzia Regionale per la Ricerca in Agricoltura, Loc. Bonassai, Olmedo, 07 100 Sassari, Italy
4 : PAPPSO-GQE-Le Moulon, INRA, Université Paris-Sud, CNRS, AgroParisTech, Université Paris-Saclay, 91 190 Gif-sur-Yvette, France
Source Science Of The Total Environment (0048-9697) (Elsevier BV), 2020-05 , Vol. 715 , P. 136834 (13p.)
DOI 10.1016/j.scitotenv.2020.136834
WOS© Times Cited 3
Keyword(s) Alexandrium pacificum, Harmful algal bloom, Proteomics, Membrane pmteome, Trace metals
Abstract

Over the past decades, the occurrence, distribution and intensity of harmful algal blooms involving the dinoflagellate Alexandrium pacificum have increased in marine coastal areas disturbed by anthropogenic inputs. This invasive species produces saxitoxin, which causes the paralytic shellfish poisoning syndrome in humans upon consumption of contaminated seafood. Blooms of A. pacificum have been reported in metal-contaminated coastal ecosystems, suggesting some ability of these microorganisms to adapt to and/or resist in metal stress conditions. This study seeks to characterize the modifications in membrane proteomes (by 2-D electrophoresis coupled to LC-MS/MS), cell growth and morphometry (measured with an inverted microscope), in response to metal stress (addition of Zn2+, Pb2+, Cu2+ and Cd2+), in two Mediterranean A. pacificum strains: SG C10-3 and TAR C5-4F, respectively isolated from the Santa Giusta Lagoon (Sardinia, Italy) and from the Tarragona seaport (Spain), both metal-contaminated ecosystems. In the SG C10-3 cultures grown in a metal cocktail, cell growth was significantly delayed, and cell size increased (22% of 37.5 μm cells after 25 days of growth). Conversely, no substantial change was observed for cell growth or cell size in the TAR C5-4F cultures grown in a metal cocktail (P > 0.10), thus indicating intraspecific variability in the responses of A. pacificum strains to metal contamination. Regardless of the conditions tested, the total number of proteins constituting the membrane proteome was significantly higher for TAR C5-4F than for SG C10-3, which may help TAR C5-4F to thrive better in contaminated conditions. For both strains, the total number of proteins constituting the membrane proteomes was significantly lower in response to metal stress (29% decrease in the SG C10-3 proteome: 82 ± 12 proteins for controls, and 58 ± 12 in metal-contaminated cultures; 17% decrease in the TAR C5-4F proteome: 101 ± 8 proteins for controls, and 84 ± 5 in metal-contaminated cultures). Moreover, regardless of the strain, proteins with significantly modified expression in response to stress were mainly down-regulated (representing 45% of the proteome for SG C10-3 and 38% for TAR C5-4F), clearly showing the harmful effects of the metals. Protein down-regulation may affect cell transport (actin and phospholipid scramblase in SG C10-3), photosynthesis (RUBISCO in SG C10-3, light-harvesting protein in TAR C5-4F, and high-CO2-inducing periplasmic protein in both strains), and finally energy metabolism (ATP synthase in both strains). However, other modifications in protein expression may confer to these A. pacificum strains a capacity for adaptation and/or resistance to metal stress conditions, for example by (i) limiting the metal entry through the plasma membrane of the SG C10-3 cells (via the down-regulation of scramblase) and/or (ii) reducing the oxidative stress generated by metals in SG C10-3 and TAR C5-4F cells (due to down-regulation of ATP-synthase).

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Chetouhi Cherif, Masseret Estelle, Satta Cecilia Teodora, Balliau Thierry, Laabir Mohamed, Jean Natacha (2020). Intraspecific variability in membrane proteome, cell growth, and morphometry of the invasive marine neurotoxic dinoflagellate Alexandrium pacificum grown in metal-contaminated conditions. Science Of The Total Environment, 715, 136834 (13p.). Publisher's official version : https://doi.org/10.1016/j.scitotenv.2020.136834 , Open Access version : https://archimer.ifremer.fr/doc/00606/71802/