Ecological divergence of a mesocosm in an eastern boundary upwelling system assessed with multi-marker environmental DNA metabarcoding

Abstract

Eastern boundary upwelling systems (EBUS) contribute a disproportionate fraction of the global fish catch relative to their size and are especially susceptible to global environmental change. Here we present the evolution of communities over 50 d in an in situ mesocosm 6 km offshore of Callao, Peru, and in the nearby unenclosed coastal Pacific Ocean. The communities were monitored using multi-marker environmental DNA (eDNA) metabarcoding and flow cytometry. DNA extracted from weekly water samples were subjected to amplicon sequencing for four genetic loci: (1) the V1–V2 region of the 16S rRNA gene for photosynthetic eukaryotes (via their chloroplasts) and bacteria; (2) the V9 region of the 18S rRNA gene for exploration of eukaryotes but targeting phytoplankton; (3) cytochrome oxidase I (COI) for exploration of eukaryotic taxa but targeting invertebrates; and (4) the 12S rRNA gene, targeting vertebrates. The multi-marker approach showed a divergence of communities (from microbes to fish) between the mesocosm and the unenclosed ocean. Together with the environmental information, the genetic data furthered our mechanistic understanding of the processes that are shaping EBUS communities in a changing ocean. The unenclosed ocean experienced significant variability over the course of the 50 d experiment, with temporal shifts in community composition, but remained dominated by organisms that are characteristic of high-nutrient upwelling conditions (e.g., diatoms, copepods, anchovies). A large directional change was found in the mesocosm community. The mesocosm community that developed was characteristic of upwelling regions when upwelling relaxes and waters stratify (e.g., dinoflagellates, nanoflagellates). The selection of dinoflagellates under the salinity-driven experimentally stratified conditions in the mesocosm, as well as the warm conditions brought about by the coastal El Niño, may be an indication of how EBUS will respond under the global environmental changes (i.e., increases in surface temperature and freshwater input, leading to increased stratification) forecast by the IPCC.