Skouri-Panet, Fériel

Abstract Magnetoreception is a remarkable ability found across a diverse range of organisms, including bacteria, birds, fish, insects, and mammals, enabling them to detect and harness the Earth’s geomagnetic field. Recently, the recruitment of biomineralizing ectosymbionts by euglenozoans was evidenced as an ecological strategy for microeukaryotes to acquire this sense. Here, we report a case of magnetosymbiosis involving a ciliate and four populations of endosymbiotic bacteria experiencing genome reduction. Among these bacteria, one group of sulphate-reducing Desulfovibrionales was found to biomineralize bundles of bullet-shaped magnetite crystals. The ciliate’s magnetotaxis mirrors that of free-living magnetotactic bacteria and euglenozoans, enabling efficient navigation in chemically stratified aquatic environments. However, in this case, magnetotaxis arises from an endosymbiotic interaction. Using a combination of optical-, confocal-, electron- and X-ray-based microscopy techniques, together with genomic analyses, these findings demonstrate that magnetosymbiosis can emerge in unicellular eukaryotic lineages through endosymbiotic integration, expanding our understanding of such interactions in aquatic ecosystems. More broadly, this work contributes to the ongoing debate on the origins of magnetoreception in eukaryotes.

Abstract Cyanobacteria have massively contributed to carbonate deposition over the geological history. They are traditionally thought to biomineralize CaCO3 extracellularly as an indirect byproduct of photosynthesis. However, the recent discovery of freshwater cyanobacteria-forming intracellular amorphous calcium carbonates (iACC) challenges this view. Despite the geochemical interest of such a biomineralization process, its molecular mechanisms and evolutionary history remain elusive. Here, using comparative genomics, we identify a new gene (ccyA) and protein family (calcyanin) possibly associated with cyanobacterial iACC biomineralization. Proteins of the calcyanin family are composed of a conserved C-terminal domain, which likely adopts an original fold, and a variable N-terminal domain whose structure allows differentiating four major types among the 35 known calcyanin homologs. Calcyanin lacks detectable full-length homologs with known function. The overexpression of ccyA in iACC-lacking cyanobacteria resulted in an increased intracellular Ca content. Moreover, ccyA presence was correlated and/or colocalized with genes involved in Ca or HCO3− transport and homeostasis, supporting the hypothesis of a functional role of calcyanin in iACC biomineralization. Whatever its function, ccyA appears as diagnostic of intracellular calcification in cyanobacteria. By searching for ccyA in publicly available genomes, we identified 13 additional cyanobacterial strains forming iACC, as confirmed by microscopy. This extends our knowledge about the phylogenetic and environmental distribution of cyanobacterial iACC biomineralization, especially with the detection of multicellular genera as well as a marine species. Moreover, ccyA was probably present in ancient cyanobacteria, with independent losses in various lineages that resulted in a broad but patchy distribution across modern cyanobacteria.