Genomic differentiation of three pico‐phytoplankton species in the Mediterranean Sea

Abstract

For more than a decade, high-throughput sequencing has transformed the study of marine planktonic communities and has highlighted the extent of protist diversity in these ecosystems. Nevertheless, little is known relative to their genomic diversity at the species-scale as well as their major speciation mechanisms. An increasing number of data obtained from global scale sampling campaigns is becoming publicly available, and we postulate that metagenomic data could contribute to deciphering the processes shaping protist genomic differentiation in the marine realm. As a proof of concept, we developed a FAIR pipeline and focused on the Mediterranean Sea to study three a priori abundant protist species: Bathycoccus prasinos, Pelagomonas calceolata and Phaeocystis cordata. We compared the genomic differentiation of each species in light of geographic, environmental and oceanographic distances. We highlighted that isolation-by-environment shapes the genomic differentiation of B. prasinos whereas P. cordata is impacted by geographic distance (i.e., isolation-by-distance). At present time, the use of metagenomics to accurately estimate the genomic differentiation of protists remains challenging since coverages are lower compared to traditional population surveys. However, our approach sheds light on Please note that this is an author-produced PDF of an article accepted for publication following peer review. The definitive publisher-authenticated version is available on the publisher Web site.ecological and evolutionary processes occurring within natural marine populations, and paves the way for future protist population metagenomic studies.

An INDEL genomic approach to explore population diversity of phytoplankton

“…As a consequence, intraspecies diversity has been poorly documented in the past in marine phytoplankton. Novel, rapid and cheap sequencing technologies have given access to Mamiellales diversity by the sequencing of the genomes of Ostreococcus isolates (Blanc-Mathieu et al 2017) or by metagenomic approaches (Leconte et al 2020, Da Silva et al 2022; Richter et al 2022) or metatranscriptomic approaches (Simmons et al 2016).…”

“…Widely distributed from the equator to arctic and antarctic poles with a marked seasonality in temperate and polar regions (Joli et al 2017, Tragin et al 2018, Lambert et al 2019, Leconte et al 2020), picoeukaryotes belonging to the order of Mamiellales ( Bathycoccus , Ostreococcus and Micromonas ) have a cosmopolitan presence illustrating a high capacity for adaptation to a wide range of contrasting environments. Novel, rapid and cheap sequencing technologies have given access to Mamiellales diversity by metagenomic approaches (Leconte et al 2020, Da Silva et al 2022, Richter et al 2022) or metatranscriptomic approaches (Simmons et al 2016), however to date, very little information is available on intraspecies diversity of Bathycoccaceae with the exception of Ostreococcus tauri (Blanc- Mathieu et al 2017). Unlike O. tauri which is usually not detectable in publicly available metagenomes, Bathycoccus is the most cosmopolitan Mamiellophyceae (de Vargas et al 2015).…”

Decoding populations in the ocean microbiome

“…17%) from diverse geographic locations and different ocean basins displayed enough coverage of the reference genome for downstream analyses [ 121 ]. Even though Bathycoccus has a relatively small genome (~ 15 Mb [ 122 ]) and displays widespread geographic distributions [ 123 ], the previous results evidence the greater difficulties of applying the metagenome-based population genomics approach to protists compared to prokaryotes [ 124 ]. The primary reason is that marine metagenomes generally encompass more prokaryotic than eukaryotic information, compounded by the inherently larger size and complexity of eukaryotic genomes.…”

“…In another work, Da Silva and colleagues investigated the genomic differentiation within three species of pico-phytoplankton in the Mediterranean Sea: Bathycoccus prasinos , Pelagomonas calceolata , and Phaeocystis cordata [ 124 ]. Here, metagenomic reads from TARA Oceans stations in the Mediterranean Sea were mapped to either reference genomes ( B. prasinos ), or transcriptomes ( P. calceolata and P. cordata ) retrieved from the Mediterranean Sea or other regions.…”

“…In general, B. prasinos displayed a higher population differentiation than P. calceolata and P. cordata in the Mediterranean Sea. In addition, results indicated that environmental selection seems to shape the population-level diversity of B. prasinos in the Mediterranean Sea, while P. cordata populations appear to be shaped by geographic distance (isolation by distance) [ 124 ]. This study demonstrates that populations of different protist species within the same functional group and with similar morphologies can exhibit varying degrees of differentiation and be influenced by distinct mechanisms, such as selection versus dispersal.…”