Sequestration of Radionuclides Radium-226 and Strontium-90 by Cyanobacteria Forming Intracellular Calcium Carbonates

Abstract

226 Ra is a naturally occurring radionuclide with a half-life of 1600 y. In 14 contrast, 90 Sr is a radionuclide of sole anthropogenic origin, produced by nuclear fission 15 reactions and has a half-life of 29 y; each of these radionuclides poses potential threats to 16 human and ecosystem health. Here, the cyanobacterium G. lithophora, capable of forming 17 intracellular amorphous calcium carbonate inclusions, was investigated for its ability to 18 uptake 226 Ra and 90 Sr. In BG-11 medium, G. lithophora accumulated 3.9 µg g -1 226 Ra within 19 144 h and 47.9 ng g -1 90 Sr within 1 h, corresponding to ~99% removal of trace radionuclides. 20 The presence of high concentration Ca 2+ in the background media solution did not inhibit 21 90 Sr and 226 Ra uptake by G. lithophora. In contrast, dead biomass of G. lithophora 22 accumulated 0.8 µg g -1 226 Ra and 8.87 ng g -1 90 Sr. Moreover, Synechocystis, a non-23 biomineralizing cyanobacteria removed only 14% and 25% of 226 Ra and 90 Sr, respectively. 24 This suggested that sequestration of 90 Sr and 226 Ra was not intrinsic to all cyanobacteria but 25 was likely a specific biological trait of G. lithophora related to the formation of intracellular 26 amorphous Ca-carbonates. The unique ability of G. lithophora to uptake 90 Sr and 226 Ra at 27 2 high rates makes it an attractive candidate for further studies involving bioremediation of 28 these radionuclides. 29 30 31 TOC image 32 33 34 Ba, with Ba/Ca and Sr/Ca atomic ratios in inclusions higher by factors of 1370 and 90 48 respectively relative to the solutions in which cells grew 3,4 . Recently, it was confirmed that 49 cyanobacteria capable of forming intracellular ACC contained a much higher content of50 alkaline earth elements (AEE) than all other cyanobacteria 5 . In addition to intracellular ACC 51 inclusions, G. lithophora also forms intracellular polyphosphate inclusions (PolyP), 52 polymers of orthophosphate which may serve as reserves of P and/or energy for cells 6 . 53 Using stable isotopes, Cam et al. showed that G. lithophora preferentially accumulated Ba 54 over Sr and finally Ca within intracellular PolyP and ACC. Currently, the origin of such a 55 surprising selectivity remains unclear. The proven ability of G. lithophora to selectively 56 sequester Sr over Ca within intracellular inclusions provides an intriguing microbial 57 framework to examine if this ability extends to radioactive AEE such as radium ( 226 Ra) and 58 radio-strontium ( 90 Sr). In the environment, 90 Sr and 226 Ra are present at trace concentrations, 59 along with excess dissolved Ca. Whether the observed selective accumulation of AEE is 60 extended to 90 Sr and 226 Ra at such low concentrations and in the presence of high 61 concentrations of Ca remains to be explored. 62 Radium-226 is a naturally occurring radioactive alkaline earth element (AEE) with a 63 half-life of 1600 y. It is one of the dominant soluble radionuclides present in groundwater 7 . 64 In the United States, 226 Ra activity in drinking water is regula...

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

“…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]. If such high accumulation abilities were proven for these ACC-producing MTB, they may similarly be suitable for designing new remediation strategies or other applications under physicochemical conditions different from those allowing the use of cyanobacteria [75].…”

“…For example, they reach up to 10% of all the operational taxonomic units (OTUs) identified in a geothermal pool at Little Hot Creek in California [24]. Due to its ability to sequester abundant alkaline earth elements within ACC, the cyanobacterium Gloeomargarita lithophora [19,25], was shown to be particularly interesting for the remediation of radionuclides such as 90 Sr and Ra [20,26]. Moreover, this cyanobacterium is the closest modern relative of plastids, questioning the possibility that this capability to sequester Ca was transferred to the first photosynthetic eukaryotes [27].…”

Microbial interaction with and tolerance of radionuclides: underlying mechanisms and biotechnological applications

“…Further examples are the accumulation of strontium into biogenic carbonate minerals by Bacillus sp. (Horiike et al, 2017) or into calcium carbonates by cyanobacteria (Mehta et al, 2019). The bacterial accumulation of technetium (Sierra et al, 2008) or plutonium by the iron reducers Geobacter sulfurreducens and Shewanella oneidensis (Renshaw et al, 2009) has been documented, as well as the sorption of plutonium by bacteria and fungi, accumulating this radionuclide intracellularly (Lujanien _ e et al, 2017).…”

The diversity of molecular mechanisms of carbonate biomineralization by bacteria

“…Boquet in 1973 showed that diverse soil bacteria produce calcium carbonates [9]. A broad diversity of carbonate mineral phases can be formed by bacteria including the different polymorphs of Ca-carbonates: calcite but also, aragonite [10] and vaterite [11], hydrated Ca-carbonates such as monohydrocalcite [12,13], amorphous (Ca, Sr, Ba, Ra)-carbonates [14,15], dolomite (Ca-Mg-CO 3 ) [16], hydromagnesite (Mg 5 (CO 3 ) 4 (OH) 2 •4H 2 O) [17], or siderite (FeCO 3 ) [18].…”