title: Unusual Versatility of the Filamentous, Diazotrophic Cyanobacterium Anabaena torulosa Revealed for Its Survival during Prolonged Uranium Exposure.
abstract: Reports on interactions between cyanobacteria and uranyl carbonate are rare. Here, we present an interesting succession of the metabolic responses employed by a marine, filamentous, diazotrophic cyanobacterium,Anabaena torulosafor its survival following prolonged exposure to uranyl carbonate extending up to 384 h at pH 7.8 under phosphate-limited conditions. The cells sequestered uranium (U) within polyphosphates on initial exposure to 100 μM uranyl carbonate for 24 to 28 h. Further incubation until 120 h resulted in (i) significant degradation of cellular polyphosphates causing extensive chlorosis and cell lysis, (ii) akinete differentiation followed by (iii) extracellular uranyl precipitation. X-ray diffraction (XRD) analysis, fluorescence spectroscopy, X-ray absorption near edge structure (XANES), and extended X-ray absorption fine structure (EXAFS) spectroscopy established the identity of the bioprecipitated uranium as a U(VI) autunite-type mineral, which settled at the bottom of the vessel. Surprisingly,A. torulosacells resurfaced as small green flakes typical of actively growing colonies on top of the test solutions within 192 to 240 h of U exposure. A consolidated investigation using kinetics, microscopy, and physiological and biochemical analyses suggested a role of inducible alkaline phosphatase activity of cell aggregates/akinetes in facilitating the germination of akinetes leading to substantial regeneration ofA. torulosaby 384 h of uranyl incubation. The biomineralized uranium appeared to be stable following cell regeneration. Altogether, our results reveal novel insights into the survival mechanism adopted byA. torulosato resist sustained uranium toxicity under phosphate-limited oxic conditions.IMPORTANCELong-term effects of uranyl exposure in cyanobacteria under oxic phosphate-limited conditions have been inadequately explored. We conducted a comprehensive examination of the metabolic responses displayed by a marine cyanobacterium,Anabaena torulosa, to cope with prolonged exposure to uranyl carbonate at pH 7.8 under phosphate limitation. Our results highlight distinct adaptive mechanisms harbored by this cyanobacterium that enabled its natural regeneration following extensive cell lysis and uranium biomineralization under sustained uranium exposure. Such complex interactions between environmental microbes such asAnabaena torulosaand uranium over a broader time range advance our understanding on the impact of microbial processes on uranium biogeochemistry.
authors.affiliation: Molecular Biology Division, Bhabha Atomic Research Centre, Trombay, Mumbai, India celin@barc.gov.in.|Homi Bhabha National Institute, Anushakti Nagar, Mumbai, India.
authors.forename: Celin
authors.initials: C
authors.lastname: Acharya
authors.affiliation: Molecular Biology Division, Bhabha Atomic Research Centre, Trombay, Mumbai, India.
authors.forename: Pallavi
authors.initials: P
authors.lastname: Chandwadkar
authors.affiliation: Atomic and Molecular Physics Division, Bhabha Atomic Research Centre, Trombay, Mumbai, India.
authors.forename: Chandrani
authors.initials: C
authors.lastname: Nayak
mesh_terms: D017033:Anabaena / Q000187:drug effects* / Q000502:physiology*; D006863:Hydrogen-Ion Concentration; D050296:Microbial Viability / Q000187:drug effects*; D013997:Time Factors; D017974:Uranium Compounds / Q000633:toxicity*
chemical_list: D017974:Uranium Compounds
keywords: biomineralization; cyanobacteria; phosphatase; polyphosphates; regeneration; uranium