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Whole-genome scanning reveals environmental selection mechanisms that shape diversity in populations of the epipelagic diatom Chaetoceros [1]

['Charlotte Nef', 'Institut De Biologie De L École Normale Supérieure', 'Ibens', 'École Normale Supérieure', 'Cnrs', 'Inserm', 'Psl Université Paris', 'Paris', 'Research Federation For The Study Of Global Ocean Systems Ecology', 'Evolution']

Date: 2022-12 

Diatoms form a diverse and abundant group of photosynthetic protists that are essential players in marine ecosystems. However, the microevolutionary structure of their populations remains poorly understood, particularly in polar regions. Exploring how closely related diatoms adapt to different environments is essential given their short generation times, which may allow rapid adaptations, and their prevalence in marine regions dramatically impacted by climate change, such as the Arctic and Southern Oceans. Here, we address genetic diversity patterns in Chaetoceros, the most abundant diatom genus and one of the most diverse, using 11 metagenome-assembled genomes (MAGs) reconstructed from Tara Oceans metagenomes. Genome-resolved metagenomics on these MAGs confirmed a prevalent distribution of Chaetoceros in the Arctic Ocean with lower dispersal in the Pacific and Southern Oceans as well as in the Mediterranean Sea. Single-nucleotide variants identified within the different MAG populations allowed us to draw a landscape of Chaetoceros genetic diversity and revealed an elevated genetic structure in some Arctic Ocean populations. Gene flow patterns of closely related Chaetoceros populations seemed to correlate with distinct abiotic factors rather than with geographic distance. We found clear positive selection of genes involved in nutrient availability responses, in particular for iron (e.g., ISIP2a, flavodoxin), silicate, and phosphate (e.g., polyamine synthase), that were further supported by analysis of Chaetoceros transcriptomes. Altogether, these results highlight the importance of environmental selection in shaping diatom diversity patterns and provide new insights into their metapopulation genomics through the integration of metagenomic and environmental data.

Funding: This work was supported by the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (Diatomic; grant agreement No. 835067 to CB and CN). Additional funding is acknowledged from the French Government “Investissements d’Avenir” Programmes MEMO LIFE (Grant ANR-10-LABX-54 to CB), Université de Recherche Paris Sciences et Lettres (PSL) (Grant ANR-125311-IDEX-0001-02 to CB); and France Génomique (ANR-10-INBS-09 to CB), and OCEANOMICS (Grant ANR-11-BTBR-0008 to CB), which were funded through Agence Nationale de la Recherche. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

As such, it is considered an important driver of carbon export and silica sinking in the modern ocean [ 4 , 36 ]. The genus displays a high level of diversity, with 239 accepted species names in Algaebase, in addition to 153 names under debate or yet to be verified ( https://www.algaebase.org , as of May 2022). It is generally accepted that the Chaetoceros genus is subdivided into the Hyalochaete and Phaeoceros subgenera, the latter including the type species Chaetoceros dichaeta, though their exact subdivision remains under debate [ 37 ]. Chaetoceros presents peculiar physiological properties that may be responsible for its prevalent distribution. For example, some Chaetoceros species have been shown to display unusually high C:N ratios unaffected by light regime and nitrogen source, suggesting a capacity to accumulate superior carbon per nitrogen units than other Arctic diatoms, while showing physiological responses similar to those of more temperate diatoms [ 38 ]. Besides its particular physiological characteristics, Chaetoceros is known to participate in a significant range of associations with a wide variety of microorganisms. The Chaetoceros phycosphere has been shown to gather a diverse set of epibiotic bacteria, the composition of which simplifies along subculturing [ 39 ], and is significantly influenced by nutrient availability and host growth stage [ 40 ]. Some associated bacteria have even been observed to favour resistance of Chaetoceros cells against viral infection and lysis compared to axenic controls [ 41 ]. Chaetoceros can be involved in photosymbioses with epibiotic peritrich and tintinnid ciliates [ 42 ], interact with nitrogen-fixing cyanobacteria in diatom–diazotroph associations [ 43 , 44 ] and is globally highly connected with other plankton members in the Tara Oceans network of planktonic associations [ 45 ]. Therefore, given the ecological significance of Chaetoceros and its prevalence in regions particularly predicted to be vulnerable to climate change, the present study focuses on describing patterns of genetic diversity and population structure of this diatom genus. To this end, we leveraged 11 metagenome-assembled genomes (MAGs) originating from the Tara Oceans expeditions [ 46 ] and that are associated with highly contextualised metadata. We aimed to answer the following questions: How are natural Chaetoceros populations structured? Is geographic distance a barrier to gene flow and, if not, what main ecological factors are correlated with Chaetoceros micro-diversification? What are the genetic functions undergoing selection among different Chaetoceros populations?

Climate change is expected to induce a range of environmental stressors on phytoplankton [ 25 ]. Among these are increased water temperature and stratification, nutrient paucity, and acidification [ 26 ]. Moreover, a recent study indicated that numerous important diatom genera, such as Chaetoceros, Porosira, and Proboscia, are predicted to be vulnerable to climate change, particularly in polar plankton communities [ 27 ]. Diatoms appear therefore to be valuable candidates to investigate the fundamental links between their genomes, physiology, and population dynamics, in light of predicted environmental changes. Understanding such principles would require access to the genome of natural diatom populations as well as precise contextual information. With the emergence of new sequencing technologies and processes to recover genomes from environmental data, either from metagenomes or single-cell genomes, it is now possible to access the genomic information of organisms by going beyond culture-dependent approaches, allowing us to gain insights into the biology and ecology of natural populations [ 28 , 29 ]. This is of particular interest for organisms for which culture conditions cannot be mimicked easily, as for instance organisms thriving in polar environments. These new techniques have enabled the scientific community to access sequences from taxa lacking significant information, such as Euryarchaeota [ 28 ], Picozoa [ 30 , 31 ], MOCHs (for Marine OCHrophytes) [ 32 ], MAST-4 (for MArine STramenopiles) [ 29 ], and rappemonads [ 33 ]. Among diatoms, the genus Chaetoceros holds a particular position as it is the most widespread, presenting a worldwide distribution from pole to pole with a prevalence at high latitudes ( Fig 1 ) [ 13 , 34 , 35 ].

Like other pelagic plankton, diatoms are thought to display high dispersion potential due to their rapid generation times and large population sizes, combined with the few apparent oceanic barriers to dispersal [ 9 , 10 ]. As a consequence, they are expected to show reduced diversity patterns and biogeographic structure due to homogenised genetic pools [ 11 ]. Instead, molecular surveys have revealed that diatom populations exhibit tremendous diversity, with more than 4,000 different operational taxonomic units (OTUs) [ 12 ], while being widely distributed across all major oceanic provinces [ 13 ] encompassing high latitudes, upwelling regions as well as stratified waters [ 14 , 15 ]. The ecological success of diatoms is undoubtedly linked to their complex evolutionary history, which was found to be sustained by horizontal gene transfers from bacteria [ 16 , 17 ], and mosaic plastid evolution derived from both red and green algae [ 18 – 20 ]. This chimeric origin led to specific physiological innovations, such as silicon utilisation for cell protection, efficient nutrient uptake systems allowing rapid responses to environmental fluctuations, a functional urea cycle, and potential carbon concentration mechanisms [ 16 , 17 , 21 ]. In contrast to these genetically encoded functions, diatom genomes themselves appear to display a wide variety of dynamics, e.g., through specific transposable elements detected in the model diatoms Thalassiosira pseudonana and Phaeodactylum tricornutum [ 16 , 22 ], alternative splicing [ 23 ], as well as gene copy number variation and mitotic recombination between homologous chromosomes [ 24 ]. Altogether, these characteristics likely fuel diatom diversity, leading to rapid diversification rates [ 17 ] while increasing their ability to respond to changing environmental conditions.

About half of primary productivity on Earth is supported by aquatic phytoplankton, a phylogenetically diverse group of photosynthetic organisms composed of eukaryotic algae and cyanobacteria that provide essential ecosystem services, from nutrient cycling and CO 2 regulation to sustaining higher trophic levels as the base of marine food webs [ 1 – 3 ] https://www.zotero.org/google-docs/?pyFXQV . Among phytoplankton, diatoms are pivotal in marine ecosystems since they account for an estimated 40% marine primary productivity and 20% global carbon fixation [ 2 ], as well as being important contributors to global carbon export [ 4 ]. Moreover, they link silicon and carbon biogeochemical cycles through the synthesis of their elaborate silicified cell walls, surrounded and embedded by glycoproteins that prevent its dissolution [ 5 , 6 ]. Diatoms are therefore key players also in the global silicon cycle, particularly in the Southern Ocean [ 7 , 8 ].

Results

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[1] Url: https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.3001893

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