Impact of the cyanobacterium Gloeomargarita lithophora on the geochemical cycles of Sr and Ba

Blondeau, Marine; Benzerara, Karim; Férard, Céline; Guigner, Jean‐Michel; Poinsot, Mélanie; Coutaud, Margot; Tharaud, Mickaël; Cordier, Laure; Skouri‐Panet, Fériel

doi:10.1016/j.chemgeo.2018.02.029

Cited by 20 publications

(25 citation statements)

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“…analyses showed the presence of Sr and Ba in the ACC granules. The accumulation of the alkaline earth elements such as Ca, Sr and Ba at a high level has been demonstrated for the ACCbiomineralizing cyanobacterium Gloeomargarita lithophora [74]. For this reason, it has been suggested that these prokaryotes could be used to remediate pollutions by alkaline earth elements [26].…”

Section: Discussionmentioning

confidence: 99%

Intracellular amorphous Ca-carbonate and magnetite biomineralization by a magnetotactic bacterium affiliated to the Alphaproteobacteria

et al. 2020

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Bacteria synthesize a wide range of intracellular submicrometer-sized inorganic precipitates of diverse chemical compositions and structures, called biominerals. Their occurrences, functions and ultrastructures are not yet fully described despite great advances in our knowledge of microbial diversity. Here, we report bacteria inhabiting the sediments and water column of the permanently stratified ferruginous Lake Pavin, that have the peculiarity to biomineralize both intracellular magnetic particles and calcium carbonate granules. Based on an ultrastructural characterization using transmission electron microscopy (TEM) and synchrotron-based scanning transmission X-ray microscopy (STXM), we showed that the calcium carbonate granules are amorphous and contained within membrane-delimited vesicles. Single-cell sorting, correlative fluorescent in situ hybridization (FISH), scanning electron microscopy (SEM) and molecular typing of populations inhabiting sediments affiliated these bacteria to a new genus of the Alphaproteobacteria. The partially assembled genome sequence of a representative isolate revealed an atypical structure of the magnetosome gene cluster while geochemical analyses indicate that calcium carbonate production is an active process that costs energy to the cell to maintain an environment suitable for their formation. This discovery further expands the diversity of organisms capable of intracellular Ca-carbonate biomineralization. If the role of such biomineralization is still unclear, cell behaviour suggests that it may participate to cell motility in aquatic habitats as magnetite biomineralization does.

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Section: Discussionmentioning

confidence: 99%

Intracellular amorphous Ca-carbonate and magnetite biomineralization by a magnetotactic bacterium affiliated to the Alphaproteobacteria

et al. 2020

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“…Several previous studies have assessed cell Ca uptake by measuring the temporal changes of dissolved extracellular Ca 2+ concentration (Blondeau, Benzerara, et al., ; Cam et al., ; Singh & Mishra, ). Yet, changes in dissolved Ca concentrations can a priori be due to (a) extracellular precipitation of Ca‐containing mineral phases, (b) adsorption at the cell surfaces and/or by surface EPS, and/or (c) Ca uptake within cells.…”

Section: Discussionmentioning

confidence: 99%

“…Washing was necessary to avoid the precipitation of salts upon drying but did not alter intracellular ACC as shown by Blondeau, Benzerara, et al. (). After washing, 3 μl of the cell suspensions was deposited on 200 mesh Formvar ™ carbon‐coated copper grids and dried at room temperature.…”

Section: Methodsmentioning

confidence: 99%

Evidence of high Ca uptake by cyanobacteria forming intracellular CaCO₃ and impact on their growth

et al. 2019

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Several species of cyanobacteria biomineralizing intracellular amorphous calcium carbonates (ACC) were recently discovered. However, the mechanisms involved in this biomineralization process and the determinants discriminating species forming intracellular ACC from those not forming intracellular ACC remain unknown. Recently, it was hypothesized that the intensity of Ca uptake (i.e., how much Ca was scavenged from the extracellular solution) might be a major parameter controlling the capability of a cyanobacterium to form intracellular ACC. Here, we tested this hypothesis by systematically measuring the Ca uptake by a set of 52 cyanobacterial strains cultured in the same growth medium. The results evidenced a dichotomy among cyanobacteria regarding Ca sequestration capabilities, with all strains forming intracellular ACC incorporating significantly more calcium than strains not forming ACC. Moreover, Ca provided at a concentration of 50 μM in BG‐11 was shown to be limiting for the growth of some of the strains forming intracellular ACC, suggesting an overlooked quantitative role of Ca for these strains. All cyanobacteria forming intracellular ACC contained at least one gene coding for a mechanosensitive channel, which might be involved in Ca influx, as well as at least one gene coding for a Ca2+/H+ exchanger and membrane proteins of the UPF0016 family, which might be involved in active Ca transport either from the cytosol to the extracellular solution or the cytosol toward an intracellular compartment. Overall, massive Ca sequestration may have an indirect role by allowing the formation of intracellular ACC. The latter may be beneficial to the growth of the cells as a storage of inorganic C and/or a buffer of intracellular pH. Moreover, high Ca scavenging by cyanobacteria biomineralizing intracellular ACC, a trait shared with endolithic cyanobacteria, suggests that these cyanobacteria should be considered as potentially significant geochemical reservoirs of Ca.

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“…This discovery was particularly surprising since cyanobacterium-mediated carbonatogenesis was before then thought to be exclusively extracellular (e.g., Riding, 2006 ; Dittrich and Sibler, 2010 ). Moreover, intracellular biomineralization of carbonates by G. lithophora was shown to be associated with the capability to strongly accumulate Sr and Ba offering some potential for remediating pollutions by these elements ( Cam et al, 2016 ; Blondeau et al, 2018 ). Finally, G. lithophora was recently proposed as the present-day closest cultured relative of primary plastids ( Ponce-Toledo et al, 2017 ), questioning the capability of their common ancestor to form intracellular CaCO 3 .…”

Section: Introductionmentioning

confidence: 99%

Amorphous Calcium Carbonate Granules Form Within an Intracellular Compartment in Calcifying Cyanobacteria

et al. 2018

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The recent discovery of cyanobacteria forming intracellular amorphous calcium carbonate (ACC) has challenged the former paradigm suggesting that cyanobacteria-mediated carbonatogenesis was exclusively extracellular. Yet, the mechanisms of intracellular biomineralization in cyanobacteria and in particular whether this takes place within an intracellular microcompartment, remain poorly understood. Here, we analyzed six cyanobacterial strains forming intracellular ACC by transmission electron microscopy. We tested two different approaches to preserve as well as possible the intracellular ACC inclusions: (i) freeze-substitution followed by epoxy embedding and room-temperature ultramicrotomy and (ii) high-pressure freezing followed by cryo-ultramicrotomy, usually referred to as cryo-electron microscopy of vitreous sections (CEMOVIS). We observed that the first method preserved ACC well in 500-nm-thick sections but not in 70-nm-thick sections. However, cell ultrastructures were difficult to clearly observe in the 500-nm-thick sections. In contrast, CEMOVIS provided a high preservation quality of bacterial ultrastructures, including the intracellular ACC inclusions in 50-nm-thick sections. ACC inclusions displayed different textures, suggesting varying brittleness, possibly resulting from different hydration levels. Moreover, an electron dense envelope of ∼2.5 nm was systematically observed around ACC granules in all studied cyanobacterial strains. This envelope may be composed of a protein shell or a lipid monolayer, but not a lipid bilayer as usually observed in other bacteria forming intracellular minerals. Overall, this study evidenced that ACC inclusions formed and were stabilized within a previously unidentified bacterial microcompartment in some species of cyanobacteria.

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Impact of the cyanobacterium Gloeomargarita lithophora on the geochemical cycles of Sr and Ba

Cited by 20 publications

References 44 publications

Intracellular amorphous Ca-carbonate and magnetite biomineralization by a magnetotactic bacterium affiliated to the Alphaproteobacteria

Intracellular amorphous Ca-carbonate and magnetite biomineralization by a magnetotactic bacterium affiliated to the Alphaproteobacteria

Evidence of high Ca uptake by cyanobacteria forming intracellular CaCO₃ and impact on their growth

Amorphous Calcium Carbonate Granules Form Within an Intracellular Compartment in Calcifying Cyanobacteria

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Impact of the cyanobacterium Gloeomargarita lithophora on the geochemical cycles of Sr and Ba

Cited by 20 publications

References 44 publications

Intracellular amorphous Ca-carbonate and magnetite biomineralization by a magnetotactic bacterium affiliated to the Alphaproteobacteria

Intracellular amorphous Ca-carbonate and magnetite biomineralization by a magnetotactic bacterium affiliated to the Alphaproteobacteria

Evidence of high Ca uptake by cyanobacteria forming intracellular CaCO3 and impact on their growth

Amorphous Calcium Carbonate Granules Form Within an Intracellular Compartment in Calcifying Cyanobacteria

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Evidence of high Ca uptake by cyanobacteria forming intracellular CaCO₃ and impact on their growth