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Bouget, F.-Y.

Publications and source records attributed to Bouget, F.-Y..

6 recordsLinked to original sources

Functional redundancy enables emergent metabolic dynamics in marine microbiomes

Understanding how marine microbiomes will respond to ongoing global change is crucial. Functional redundancy, the capacity of different microbes to perform the same function, is considered a key mechanism underpinning the stability and resilience of the ocean microbiome. Although the extent of functional redundancy remains debated, investigating its manifestation in environmentally similar and interconnected microbial communities may provide critical insights into its role in shaping microbial community dynamics. We hypothesized that examining the long-term synchrony and rhythmicity of temperate microbial communities in such locations could provide insight into the role of functional redundancy. High functional redundancy at the community level would manifest as rhythmic and synchronous metabolic functions across sites, even in the absence of synchrony or rhythmicity at finer organizational levels, such as individual genes or taxa, thereby contributing to community resilience. Conversely, low functional redundancy would imply that synchrony and rhythmicity extend to both the contributing genes and taxa, suggesting a greater vulnerability of the community to environmental variability. To test this framework, we analyzed the long-term synchrony and rhythmicity of two marine-coastal microbiomes in the Mediterranean Sea, separated by approximately 150 km and connected by a dominant southwest current. Monthly collected metagenomes from a seven-year period were examined at the levels of metabolic functions (e.g., KEGG pathways), predicted genes (open reading frames), and taxa. We found functions, genes, and taxa exhibiting high, low, or anti-synchrony, as well as displaying rhythmic or non-rhythmic patterns. Although rhythmic behavior was observed on average across all organizational levels, consistent with the seasonal dynamics expected in temperate Mediterranean waters, average synchrony across microbiomes remained low. Focusing specifically on 45 markers of key biogeochemical functions, we revealed that several functions exhibited high synchrony and rhythmicity, in sharp contrast to the low synchrony and rhythmicity among the most abundant genes and taxa contributing to those functions. This suggests that functional redundancy and complementary dynamics at lower organizational levels, with distinct taxa contributing to key metabolic functions at different times, lead to rhythmic and synchronous dynamics at higher levels through emergent self-organization. Together, our results highlight functional redundancy and emergent self-organized dynamics as key mechanisms supporting the stability and resilience of marine microbiomes under environmental change.

ecology↗

Circadian regulation of key physiological processes by the RITMO1 clock protein in the marine diatom Phaeodactylum tricornutum

O_LIPhasing biological and physiological processes to periodic light-dark cycles is crucial for the life of most organisms. Marine diatoms, as many phytoplanktonic species, exhibit biological rhythms, yet their molecular timekeepers remain largely uncharacterized. Recently, the bHLH-PAS protein RITMO1 has been proposed to act as a regulator of circadian rhythms. C_LIO_LIIn this study, we first determined the physiological conditions to monitor circadian clock activity and its perturbation in the diatom model species Phaeodactylum tricornutum by using cell fluorescence as a circadian output. Employing ectopic overexpression, targeted gene mutagenesis, and functional complementation, we then investigated the role of RITMO1 in various circadian processes. C_LIO_LIOur findings reveal that RITMO1 significantly influences the P. tricornutum circadian rhythms not only of cellular fluorescence, but also of photosynthesis and of the expression of clock-controlled genes, including transcription factors and putative clock input/output components. RITMO1 effects on rhythmicity are unambiguously detectable under free running conditions. C_LIO_LIBy uncovering the complex regulation of biological rhythms in P. tricornutum, these results provide a key step in understanding the endogenous regulators of phytoplankton physiological responses to environmental changes. Furthermore, these studies position diatoms as instrumental and novel model systems for elucidating key mechanistic principles of oscillator functions in marine ecosystems. C_LI

molecular biology↗

Biological and genomic resources for the cosmopolitan phytoplankton Bathycoccus: Insights into genetic diversity and major structural variations

1.Population-scale genome sequencing has become essential for exploring genetic diversity and adaptation, particularly in land plants. In contrast, eukaryotic phytoplankton resources remain limited to model reference genomes or community-level metagenomics, leaving a gap in understanding intraspecific variation and evolutionary processes. To address this, we developed a comprehensive biological and genomic resource for the cosmopolitan and ecologically important genus Bathycoccus. Extensive metagenomic data from across the world Ocean are available for this genus, and previous studies have identified four Bathycoccus species and reconstructed 34 metagenome-assembled genomes. Here we report 28 high-quality strain genome sequences using a combination of Oxford Nanopore Technologies long reads and Illumina short reads and associated biological resources. These include 24 Bathycoccus prasinos strains spanning a latitudinal gradient from 40{degrees} to 78{degrees}N, a reference genome for Bathycoccus calidus, and three genomes of the recently identified B3 clade, which we propose as the Bathycoccus catiminus species. Comparative analyses of sequenced genomes with MAGs highlight the complementarity between resources: while MAGs capture environmental diversity and uncover uncultured taxa, the cultured strain genomes provide complete, non-chimeric high-quality assemblies that resolve structural variations and haplotype-level diversity not detected in MAGs. These include the large outlier chromosome (BOC), a putative sexual chromosome revealing a second mating type, and extensive variability in the small outlier chromosome (SOC), associated with viral resistance and genome plasticity. Together, these biological and genomic resources establish Bathycoccus prasinos as a powerful model for studying diversity, adaptation, and evolution of eukaryotic phytoplankton in the ocean, complementing existing global metagenomic datasets. 2. Significance statementEukaryotic phytoplankton are key to ocean ecosystems, yet their intraspecific genomic diversity is poorly understood. We present 28 high-quality genomes and their annotations of the cosmopolitan microalga Bathycoccus, revealing whole genome structural variations, chromosomal haplotype diversity linked to mating and viral resistance, and offering a genomic framework that complements metagenomic data to establish this picoalga as a model for functional and ecological studies.

genomics↗

Population dynamics of the cosmopolitan eukaryotic picophytoplankton Bathycoccusduring seasonal blooms in the bay of Banyuls sur Mer (North Western Mediterraneansea)

BackgroundAlthough metabarcoding and metagenomic approaches have generated large datasets on worldwide phytoplankton species diversity, the intraspecific genetic diversity underlying the genetic adaptation of marine phytoplankton to specific environmental niches remains largely unexplored. This is mainly due to the lack of biological resources and tools for monitoring the dynamics of this diversity in space and time. ResultsTo gain insight into population diversity, a novel method based on INDEL markers was developed on Bathycoccus prasinos (Mamiellophyceae), an abundant and cosmopolitan species with strong seasonal patterns. Long read sequencing was first used to characterise structural variants among the genomes of six B. prasinos strains sampled from geographically distinct regions in the world ocean. Markers derived from identified insertions/deletions were validated by PCR then used to genotype 55 B. prasinos strains isolated during the winter bloom 2018-2019 in the bay of Banyuls-sur-Mer (Mediterranean Sea, France). This led to their classification into eight multi-loci genotypes and the sequencing of strains representative of local diversity, further improving the available genetic diversity of B. prasinos. Finally, selected markers were directly tracked on environmental DNA sampled during 3 successive blooms from 2018 to 2021, showcasing a fast and cost-effective approach to follow local population dynamics. ConclusionsThis method, which involves (i) pre-identifying the genetic diversity of B. prasinos in environmental samples by PCR, (ii) isolating cells from selected environmental samples and (iii) identifying genotypes representative of B. prasinos diversity for sequencing, can be used to comprehensively describe the diversity and population dynamics not only in B. prasinos but also potentially in other generalist phytoplankton species.

ecology↗

In situ community dynamics influences the temperature- and light- dependent succession of seasonal phytoplankton

Temperature and light play a crucial role in regulating phytoplankton blooms in the Ocean. To assess the importance of these two parameters experimentally, microcosms were conducted on seven picoplankton communities (<3 m) sampled in December, March, June and September 2015 and 2016 in the North Western Mediterranean Sea. Each community was exposed to 4 realistic seasonal conditions (December, March, June and September). Metabarcoding was used to investigate the eukaryotic diversity in the 56 microcosms experiments in parallel to high-frequency monitoring of environmental diversity in the sea. The three major lineages identified were the Stramenopiles, Alveolata and Archaeplastida. Overall, the five-day incubations were not sufficient to reshape the initial microbial communities completely. The microcosm outcome was strongly influenced by the dynamics of phytoplankton starting communities. In pre-bloom conditions, phytoplanktonic species were the most sensitive to temperature and light conditions. During a bloom, species belonging to diatoms or Chlorodendrophyceae usually did not respond to light and temperature in microcosms and continued to bloom independently of the applied seasonal condition. Together, these results suggest that light and temperature seasonal conditions play a crucial role in regulating phytoplankton dynamics in pre-bloom conditions and biotic interactions may be preponderant in bloom and post-bloom conditions.

ecology↗

A bHLH-PAS protein regulates light-dependent rhythmic processes in the marine diatom Phaeodactylum tricornutum

Periodic light-dark cycles govern the timing of basic biological processes in organisms inhabiting land as well as the sea, where life evolved. Although prominent marine phytoplanktonic organisms such as diatoms show robust diurnal rhythms in growth, cell cycle and gene expression, the molecular foundations controlling these processes are still obscure. By exploring the regulatory landscape of diatom diurnal rhythms, we unveil the function of a Phaeodactylum tricornutum bHLH-PAS protein, PtbHLH1a, in the regulation of light-dependent diurnal rhythms. Peak expression of PtbHLH1a mRNA occurs toward the end of the light period and it adjusts to photoperiod changes. Ectopic over-expression of PtbHLH1a results in lines showing a phase shift in diurnal cell fluorescence, compared to the wild-type cells, and with altered cell cycle progression and gene expression. Reduced oscillations in gene expression are also observed in overexpression lines compared to wild-type in continuous darkness, showing that the regulation of rhythmicity by PtbHLH1a is not directly dependent on light inputs and cell division. PtbHLH1a homologs are widespread in diatom genomes which may indicate a common function in many species. This study adds new elements to understand diatom biology and ecology and offers new perspectives to elucidate timekeeping mechanisms in marine organisms belonging to a major, but underinvestigated branch of the tree of life.\n\nSIGNIFICANCE STATEMENTMost organisms experience diurnal light-dark changes and show rhythms of basic biological processes such that they occur at optimal times of the day. The ocean harbours a huge diversity of organisms showing light-dependent rhythms, but their molecular foundations are still largely unknown. In this study, we discover a novel protein, PtbHLH1a that regulates cell division, gene expression and the diurnal timing of these events in the marine diatom Phaedoactylum tricornutum. The identification of PtbHLH1a-like genes in many diatom species suggests a conserved function in diurnal rhythm regulation in the most species-rich group of algae in the ocean. This study unveils critical features of diatom biology and advances the field of marine rhythms and their environmental regulation.

molecular biology↗