From communities to single cells: Exploring diversity and ecophysiology of marine microbes with a focus on coccolithophores

Abstract

Microeukaryotes form the basis of the marine food web and play a pivotal role in marine biogeochemical processes. However, for many clades, ecological niches and inherent patterns of diversity and abundance remain poorly understood. One of the most charismatic microbial taxa are the coccolithophores, unicellular phytoplankton characterized by the production of calcite coccoliths and important contributors to microbial standing stocks. This study set out to investigate the biogeography and ecophysiology of marine microeukaryotes, focusing on coccolithophores and their elusive life cycle. Environmental sampling, culture experiments, omics techniques, and bioinformatics were integrated to elucidate the diversity and functional attributes of microbial communities. An investigation of the distribution and physiology of marine microeukaryotes in the Pacific and Indian sector of the Great Calcite Belt in the Southern Ocean, an area of particularly high coccolithophore abundance, revealed that microbial communities are strongly influenced by environmental gradients associated with frontal and mesoscale systems. However, distinct clades exhibited significant disparities in their degree of constraint, underscoring the necessity for a more profound understanding of the underlying physiology across different taxa. The lack of coccolithophore diversity revealed by broad eukaryotic 18S metabarcoding raised concerns about the underrepresentation of this group in global genomic explorations. Re-examining the area with a combination of improved genetic markers and morphological taxonomy, revealed a much higher degree of coccolithophore diversity. This underscores the limitations of current environmental DNA methodologies, highlighting the need for supplementary techniques and advancements in gene markers and reference libraries. The morphological examination of coccolithophores further unveiled novel insights into their elusive haplo-diplontic life cycle. The finding of a new combination coccosphere, a transitionary life phase, raised important questions regarding genetic variability and cryptic speciation in coccolithophores. Further examining the underlying ecophysiology of the coccolithophore life cycle, particularly by using proteomics approaches, has highlighted life cycle-specific mechanisms and traits. This investigation expanded our understanding beyond the well-studied Gephyrocapsa (formerly Emiliania) huxleyi, elucidating the evolution of calcification-related genes and investigating the broader physiological and evolutionary significance of the findings through culture experiments and gene phylogenies. Overall, this thesis provides a comprehensive understanding of marine microeukaryotes, highlighting their intricate dynamics across biogeographic regions and offering insights into their ecological adaptations. Through a multidisciplinary approach, it advances our knowledge of microbial communities in remote oceanic realms, with implications for broader ecological and biogeochemical processes.

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ORCID for Toby Tyrrell: orcid.org/0000-0002-1002-1716

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