Sediment archives reveal irreversible shifts in plankton communities after World War II and agricultural pollution

• Published in: Current biology 2021-06, Vol.31 (12), p.2682-2689.e7
• Main Authors: Siano, Raffaele, Lassudrie, Malwenn, Cuzin, Pierre, Briant, Nicolas, Loizeau, Véronique, Schmidt, Sabine, Ehrhold, Axel, Mertens, Kenneth Neil, Lambert, Clément, Quintric, Laure, Noël, Cyril, Latimier, Marie, Quéré, Julien, Durand, Patrick, Penaud, Aurélie
• Format: Article
• Language: English
• Subjects: Biodiversity; coastal ecology; community shifts; dinoflagellates; Dinoflagellida - genetics; Ecosystem; Environmental Sciences; environmental sedimentary ancient DNA; Geologic Sediments; Humans; metabarcoding; paleoecology; Plankton - genetics; pollution; protists; Retrospective Studies; sedaDNA; sediment; stramenopiles; World War II
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2021.03.079

To evaluate the stability and resilience1 of coastal ecosystem communities to perturbations that occurred during the Anthropocene,2 pre-industrial biodiversity baselines inferred from paleoarchives are needed.3,4 The study of ancient DNA (aDNA) from sediments (sedaDNA)5 has provided valuable information about past dynamics of microbial species6–8 and communities9–18 in relation to ecosystem variations. Shifts in planktonic protist communities might significantly affect marine ecosystems through cascading effects,19–21 and therefore the analysis of this compartment is essential for the assessment of ecosystem variations. Here, sediment cores collected from different sites of the Bay of Brest (northeast Atlantic, France) allowed ca. 1,400 years of retrospective analyses of the effects of human pollution on marine protists. Comparison of sedaDNA extractions and metabarcoding analyses with different barcode regions (V4 and V7 18S rDNA) revealed that protist assemblages in ancient sediments are mainly composed of species known to produce resting stages. Heavy-metal pollution traces in sediments were ascribed to the World War II period and coincided with community shifts within dinoflagellates and stramenopiles. After the war and especially from the 1980s to 1990s, protist genera shifts followed chronic contaminations of agricultural origin. Community composition reconstruction over time showed that there was no recovery to a Middle Ages baseline composition. This demonstrates the irreversibility of the observed shifts after the cumulative effect of war and agricultural pollutions. Developing a paleoecological approach, this study highlights how human contaminations irreversibly affect marine microbial compartments, which contributes to the debate on coastal ecosystem preservation and restoration. [Display omitted] •Protist paleocommunities are mainly composed of resting cysts•Anthropogenic contamination caused irreversible shifts in protist communities•Protist division shifts coincided with pollution accumulated during World War II•Variation in protist genus abundances followed chronic agricultural contamination Using a multidisciplinary paleoecological approach, Siano et al. show irreversible shifts in coastal protist communities coinciding with anthropogenic pollution accumulated during the XXth century. This work highlights the importance of retrospective analyses for the evaluation of marine coastal ecosystem stability and resilience.