Interaction of uranium with a filamentous, heterocystous, nitrogen-fixing cyanobacterium, Anabaena torulosa

Acharya, Celin; Chandwadkar, Pallavi; Apte, Shree Kumar

doi:10.1016/j.biortech.2012.03.068

Cited by 41 publications

(20 citation statements)

References 28 publications

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“…1A). These results are in agreement with our previous observations on uranyl interactions with this cyanobacterium (42,61). The compartmentalization of uranium in polyphosphates in A. torulosa within 24 h of U exposure (Fig.…”

Section: Discussionsupporting

confidence: 93%

“…The observed chlorosis in U-exposed A. torulosa cells was most likely due to the degradation of photosynthetic pigments and is a known consequence of heavy-metal exposure in cyanobacteria (41). Previously, we witnessed ϳ10% inhibition in the growth of this strain when exposed to 100 M U for 24 to 30 h compared with that in control U-unexposed conditions (42). No cell lysis was observed and the chlorophyll a contents did not change measurably within 24 to 30 h of U exposure under phosphatelimited conditions (Fig.…”

Section: Resultsmentioning

confidence: 80%

“…The compartmentalization of uranium in polyphosphates in A. torulosa within 24 h of U exposure (Fig. 1A and 3C) made U less available to the cells, thus minimizing U toxicity (42). The incorporation of heavy metals into polyphosphates as a mechanism of metal detoxification has been reported in Anabaena cells (41).…”

Section: Discussionmentioning

confidence: 84%

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Unusual Versatility of the Filamentous, Diazotrophic Cyanobacterium Anabaena torulosa Revealed for Its Survival during Prolonged Uranium Exposure

Acharya

Chandwadkar

Nayak

2017

Appl Environ Microbiol

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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 torulosa for 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 M 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. torulosa cells 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 of A. torulosa by 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 by A. torulosa to resist sustained uranium toxicity under phosphate-limited oxic conditions. IMPORTANCE Long-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 as Anabaena torulosa and uranium over a broader time range advance our understanding on the impact of microbial processes on uranium biogeochemistry.KEYWORDS biomineralization, cyanobacteria, phosphatase, polyphosphates, regeneration, uranium M icroorganisms have existed on earth for at least 3.5 billion years (1) and are the most successful life forms to date (2). They have been exposed to their immediate environments comprising essential elements or complex mixtures of naturally occur-

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Section: Discussionsupporting

confidence: 93%

Section: Resultsmentioning

confidence: 80%

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Unusual Versatility of the Filamentous, Diazotrophic Cyanobacterium Anabaena torulosa Revealed for Its Survival during Prolonged Uranium Exposure

Acharya

Chandwadkar

Nayak

2017

Appl Environ Microbiol

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“…ioremediation strategies, such as bioreduction (1-3), biosorption (4)(5)(6)(7)(8), bioaccumulation (9,10), and bioprecipitation (5,11,12,13), have been studied for their potential to immobilize U from solutions. There is also a large body of work on microbial interactions with uranium relevant to environmental in situ bioremediation.…”

mentioning

confidence: 99%

Interaction of Uranium with Bacterial Cell Surfaces: Inferences from Phosphatase-Mediated Uranium Precipitation

Kulkarni

Misra

Gupta

et al. 2016

Appl Environ Microbiol

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Deinococcus radiodurans and Escherichia coli expressing either PhoN, a periplasmic acid phosphatase, or PhoK, an extracellular alkaline phosphatase, were evaluated for uranium (U) bioprecipitation under two specific geochemical conditions (GCs): (i) a carbonate-deficient condition at near-neutral pH (GC1), and (ii) a carbonate-abundant condition at alkaline pH (GC2). Transmission electron microscopy revealed that recombinant cells expressing PhoN/PhoK formed cell-associated uranyl phosphate precipitate under GC1, whereas the same cells displayed extracellular precipitation under GC2. These results implied that the cell-bound or extracellular location of the precipitate was governed by the uranyl species prevalent at that particular GC, rather than the location of phosphatase. MINTEQ modeling predicted the formation of predominantly positively charged uranium hydroxide ions under GC1 and negatively charged uranyl carbonate-hydroxide complexes under GC2. Both microbes adsorbed 6-to 10-fold more U under GC1 than under GC2, suggesting that higher biosorption of U to the bacterial cell surface under GC1 may lead to cell-associated U precipitation. In contrast, at alkaline pH and in the presence of excess carbonate under GC2, poor biosorption of negatively charged uranyl carbonate complexes on the cell surface might have resulted in extracellular precipitation. The toxicity of U observed under GC1 being higher than that under GC2 could also be attributed to the preferential adsorption of U on cell surfaces under GC1. This work provides a vivid description of the interaction of U complexes with bacterial cells. The findings have implications for the toxicity of various U species and for developing biological aqueous effluent waste treatment strategies. IMPORTANCEThe present study provides illustrative insights into the interaction of uranium (U) complexes with recombinant bacterial cells overexpressing phosphatases. This work demonstrates the effects of aqueous speciation of U on the biosorption of U and the localization pattern of uranyl phosphate precipitated as a result of phosphatase action. Transmission electron microscopy revealed that location of uranyl phosphate (cell associated or extracellular) was primarily influenced by aqueous uranyl species present under the given geochemical conditions. The data would be useful for understanding the toxicity of U under different geochemical conditions. Since cell-associated precipitation of metal facilitates easy downstream processing by simple gravitybased settling down of metal-loaded cells, compared to cumbersome separation techniques, the results from this study are of considerable relevance to effluent treatment using such cells. Bioremediation strategies, such as bioreduction (1-3), biosorption (4-8), bioaccumulation (9, 10), and bioprecipitation (5, 11, 12, 13), have been studied for their potential to immobilize U from solutions. There is also a large body of work on microbial interactions with uranium relevant to environmental in situ bioremediation. The...

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“…Majority of the published reports of intracellular accumulation have shown the formation of uranyl phosphates as a result of precipitation of uranium and phosphate within the cells (VanEngelen et al 2010;Suzuki and Banfield 2004). Uranium immobilization by acid-soluble, surface-associated polyphosphates demonstrated a novel uranium sequestration phenomenon in a marine, filamentous cyanobacterium, Anabaena torulosa (Acharya et al 2012;Acharya and Apte 2013b).…”

Section: Bioaccumulationmentioning

confidence: 98%

Uranium Bioremediation: Approaches and Challenges

Acharya

2015

Soil Biology

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Interaction of uranium with a filamentous, heterocystous, nitrogen-fixing cyanobacterium, Anabaena torulosa

Cited by 41 publications

References 28 publications

Unusual Versatility of the Filamentous, Diazotrophic Cyanobacterium Anabaena torulosa Revealed for Its Survival during Prolonged Uranium Exposure

Unusual Versatility of the Filamentous, Diazotrophic Cyanobacterium Anabaena torulosa Revealed for Its Survival during Prolonged Uranium Exposure

Interaction of Uranium with Bacterial Cell Surfaces: Inferences from Phosphatase-Mediated Uranium Precipitation

Uranium Bioremediation: Approaches and Challenges

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