Skouri-Panet, F. | Search bioRxiv

bioRxiv2022

Description of Gloeomargarita ahousahtiae sp. nov., a thermophilic member of the order Gloeomargaritales with intracellular carbonate inclusions

A unicellular cyanobacterium, strain VI4D9, was isolated from thermophilic microbial mats thriving in a hot spring of the Ahousaht territory of Vancouver Island, Canada. The cells were elongated rods (5.1 m in length and 1.2 m in width on average). Their UV-visible absorption spectra revealed that they contain chlorophyll a, phycocyanin, and carotenoids. Transmission electron microscopy showed the presence of thylakoids concentrated on one side of the cells. The strain grew within a temperature range of 37-50{degrees}C, with an optimum at 45{degrees}C. Its genome had a size of 3,049,282 bp and a DNA G+C content of 51.8 mol%. The cells contained numerous intracellular spherical granules easily visible under scanning electron microscopy. Energy-dispersive x-ray spectroscopy revealed that these granules were made of Ca-, Ba- and Sr-containing carbonates. A phylogenetic 16S rRNA gene tree robustly placed this strain as sister to several environmental sequences and the described species Gloeomargarita lithophora, also characterized by the possession of intracellular carbonate inclusions. We consider strain VI4D9 to represent a new Gloeomargarita species based on its marked phenotypic differences with G. lithophora, notably, its thermophilic nature and different thylakoid organization. We propose the name Gloeomargarita ahousahtiae sp. nov. for this newly isolated thermophilic cyanobacterium. The type strain is VI4D9 (Culture Collection of Algae and Protozoa strain 1472/1; Laboratorio de Algas Continentales Mexico strain LAC 140). G. ahousahtiae is the second species described within the recently discovered order Gloeomargaritales.

microbiology↗

bioRxiv2021

A new gene family diagnostic for intracellular biomineralization of amorphous Ca-carbonates by cyanobacteria

Cyanobacteria have massively contributed to carbonate deposit formation 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 (calcyanin) family specifically associated with cyanobacterial iACC biomineralization. Calcyanin is composed of a conserved C-terminal domain, which likely adopts an original fold, and a variable N-terminal domain whose structure allows differentiating 4 major types among the 35 known calcyanin homologues. Calcyanin lacks detectable full-length homologs with known function. Yet, genetic and comparative genomic analyses suggest a possible involvement in Ca homeostasis, making this gene family a particularly interesting target for future functional studies. Whatever its function, this new gene family appears as a gene diagnostic of intracellular calcification in cyanobacteria. By searching for ccyA in publicly available genomes, we identified 13 additional cyanobacterial strains forming iACC. This significantly 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. Phylogenetic analyses indicate that iACC biomineralization is ancient, with independent losses in various lineages and some HGT cases that resulted in the broad but patchy distribution of calcyanin across modern cyanobacteria. Overall, iACC biomineralization emerges as a new case of genetically controlled biomineralization in bacteria. Significance statementFew freshwater species of Cyanobacteria have been known to mineralize amorphous CaCO3 (ACC) intracellularly. Despite the geochemical interest of this biomineralization, its evolutionary history and molecular mechanism remain poorly known. Here, we report the discovery of a new gene family that has no homolog with known function, which proves to be a good diagnostic marker of this process. It allowed to find cyanobacteria in several phyla and environments such as seawater, where ACC biomineralization had not been reported before. Moreover, this gene is ancient and was independently lost in various lineages with some later horizontal transfers, resulting in a broad and patchy phylogenetic distribution in modern cyanobacteria.

evolutionary biology↗