Arsenic metabolism in cyanobacteria

2016 ◽  
Vol 13 (4) ◽  
pp. 577 ◽  
Author(s):  
Shin-ichi Miyashita ◽  
Chisato Murota ◽  
Keisuke Kondo ◽  
Shoko Fujiwara ◽  
Mikio Tsuzuki

Environmental context Cyanobacteria are ecologically important, photosynthetic organisms that are widely distributed throughout the environment. They play a central role in arsenic transformations in terms of both mineralisation and formation of organoarsenic species as the primary producers in aquatic ecosystems. In this review, arsenic resistance, transport and biotransformation in cyanobacteria are reviewed and compared with those in other organisms. Abstract Arsenic is a toxic element that is widely distributed in the lithosphere, hydrosphere and biosphere. Some species of cyanobacteria can grow in high concentrations of arsenate (pentavalent inorganic arsenic compound) (100mM) and in low-millimolar concentrations of arsenite (trivalent inorganic arsenic compound). Arsenate, which is a molecular analogue of phosphate, is taken up by cells through phosphate transporters, and inhibits oxidative phosphorylation and photophosphorylation. Arsenite, which enters the cell through a concentration gradient, shows higher toxicity than arsenate by binding to sulfhydryl groups and impairing the functions of many proteins. Detoxification mechanisms for arsenic in cyanobacterial cells include efflux of intracellular inorganic arsenic compounds, and biosynthesis of methylarsonic acid and dimethylarsinic acid through methylation of intracellular inorganic arsenic compounds. In some cyanobacteria, ars genes coding for an arsenate reductase (arsC), a membrane-bound protein involved in arsenic efflux (arsB) and an arsenite S-adenosylmethionine methyltransferase (arsM) have been found. Furthermore, cyanobacteria can produce more complex arsenic species such as arsenosugars. In this review, arsenic metabolism in cyanobacteria is reviewed, compared with that in other organisms. Knowledge gaps remain regarding both arsenic transport (e.g. uptake of methylated arsenicals and excretion of arsenate) and biotransformation (especially production of lipid-soluble arsenicals). Further studies in these areas are required, not only for a better understanding of the role of cyanobacteria in the circulation of arsenic in aquatic environments, but also for their application to arsenic bioremediation.


1983 ◽  
Vol 40 (8) ◽  
pp. 1254-1257 ◽  
Author(s):  
M. D. Baker ◽  
P. T. S. Wong ◽  
Y. K. Chau ◽  
C. I. Mayfield ◽  
W. E. Inniss

Isolates from four genera of freshwater green algae were capable of methylating sodium arsenite in lake water and Bold's basal medium. Analysis of the liquid phase of the methylation flasks revealed the presence of methylarsonic acid, dimethylarsinic acid, and trimethylarsine oxide. Volatile arsine and methylarsines were not detected in the headspace gases presumably because of the inability of the algae to reduce completely the methylated–arsenic species. Although the algae varied with respect to their methylating abilities, the levels of methylated–arsenic compounds were always significantly higher when the algae were grown in lake water. This may have been due to the lower phosphate concentration in the lake water. We suggest that arsenic methylation by green algae constitutes an additional source for the formation and cycling of organo-arsenic compounds in freshwater ecosystems.



2002 ◽  
Vol 66 (2) ◽  
pp. 250-271 ◽  
Author(s):  
Ronald Bentley ◽  
Thomas G. Chasteen

SUMMARY A significant 19th century public health problem was that the inhabitants of many houses containing wallpaper decorated with green arsenical pigments experienced illness and death. The problem was caused by certain fungi that grew in the presence of inorganic arsenic to form a toxic, garlic-odored gas. The garlic odor was actually put to use in a very delicate microbiological test for arsenic. In 1933, the gas was shown to be trimethylarsine. It was not until 1971 that arsenic methylation by bacteria was demonstrated. Further research in biomethylation has been facilitated by the development of delicate techniques for the determination of arsenic species. As described in this review, many microorganisms (bacteria, fungi, and yeasts) and animals are now known to biomethylate arsenic, forming both volatile (e.g., methylarsines) and nonvolatile (e.g., methylarsonic acid and dimethylarsinic acid) compounds. The enzymatic mechanisms for this biomethylation are discussed. The microbial conversion of sodium arsenate to trimethylarsine proceeds by alternate reduction and methylation steps, with S-adenosylmethionine as the usual methyl donor. Thiols have important roles in the reductions. In anaerobic bacteria, methylcobalamin may be the donor. The other metalloid elements of the periodic table group 15, antimony and bismuth, also undergo biomethylation to some extent. Trimethylstibine formation by microorganisms is now well established, but this process apparently does not occur in animals. Formation of trimethylbismuth by microorganisms has been reported in a few cases. Microbial methylation plays important roles in the biogeochemical cycling of these metalloid elements and possibly in their detoxification. The wheel has come full circle, and public health considerations are again important.



2002 ◽  
Vol 53 (6) ◽  
pp. 971 ◽  
Author(s):  
R. Tukai ◽  
W. A. Maher ◽  
I. J. McNaught ◽  
M. J. Ellwood ◽  
M. Coleman

Arsenic concentrations were measured in thirteen macroalgal species from Sydney, Australia. Brown macroalgae contained, on average, more arsenic (range, mean ± s.e.: 5–173 μg g–1, 39 ± 4 μg g–1) than either green (0.12–30.2 μg g–1, 10.7 ± 0.7 μg g–1) or red macroalgae (0.11–16.9 μg g–1, 4.3 ± 0.3 μg g–1). Despite the overlap in arsenic concentrations between different macroalgal species, inter-species arsenic variation was apparent with arsenic concentrations following the order brown > green > red macroalgal species. It was concluded that the main contribution to the variation in arsenic concentration was from natural variability expected to occur between individuals of any species as a result of physiological differences.Most of the arsenic compounds in macroalgae (70–108%) could be extracted using methanol/water mixtures, with 38–95% of the arsenic compounds present in characterizable forms. All macroalgal species contained arsenoribosides (9–99%). The distribution of arsenoribosides followed a general pattern; glycerol-arsenoriboside and phosphate-arsenoriboside were common to all macroalgal species. Sulfonate-arsenoriboside and sulfate-arsenoriboside were found in brown macroalgal species and one red macroalgal species. Six macroalgal species contained high concentrations of inorganic arsenic (14.2–62.9%) and four species contained high concentrations of dimethylarsinic acid (13.3–41.1%). The variation in the distribution of arsenic compounds in marine macroalgal species appears to be related to taxonomic differences in storage and structural polysaccharides.



1998 ◽  
Vol 44 (3) ◽  
pp. 539-550 ◽  
Author(s):  
Mingsheng Ma ◽  
X Chris Le

Abstract We developed and evaluated a method for the determination of μg/L concentrations of individual arsenic species in urine samples. We have mainly studied arsenite [As(III)], arsenate [As(V)], monomethylarsonic acid (MMAA), and dimethylarsinic acid (DMAA) because these are the most commonly used biomarkers of exposure by the general population to inorganic arsenic and because of concerns over these arsenic species on their toxicity and carcinogenicity. We have also detected five unidentified urinary arsenic species resulting from the metabolism of arsenosugars. We combined ion pair liquid chromatography with on-line hydride generation and subsequent atomic fluorescence detection (HPLC/HGAFS). Detection limits, determined as three times the standard deviation of the baseline noise, are 0.8, 1.2, 0.7, and 1.0 μ/L arsenic for arsenite, arsenate, MMAA, and DMAA, respectively. These correspond to 16, 24, 14, and 20 pg of arsenic, respectively, for a 20-μL sample injected for analysis. The excellent detection limit enabled us to determine trace concentrations of arsenic species in urine samples from healthy subjects who did not have excess exposure to arsenic. There was no need for any sample pretreatment step. We used Standard Reference Materials, containing both normal and increased concentrations of arsenic, to validate the method. Interlaboratory studies with independent techniques also confirmed the results obtained with the HPLC/HGAFS method. We demonstrated an application of the method to the determination of arsenic species in urine samples after the ingestion of seaweed by four volunteers. We observed substantial increases of DMAA concentrations in the samples collected from the volunteers after the consumption of seaweed. The increase of urinary DMAA concentration is due to the metabolism of arsenosugars that are present in the seaweed. Our results suggest that the commonly used biomarkers of exposure to inorganic arsenic, based on the measurement of arsenite, arsenate, MMAA, and DMAA, are not reliable when arsenosugars are ingested from the diet.



Biomolecules ◽  
2020 ◽  
Vol 10 (9) ◽  
pp. 1351
Author(s):  
Nirmal K. Roy ◽  
Anthony Murphy ◽  
Max Costa

Arsenic occurs naturally in the environment, and exists predominantly as inorganic arsenite (As (III) and arsenate As (V)). Arsenic contamination of drinking water has long been recognized as a major global health concern. Arsenic exposure causes changes in skin color and lesions, and more severe health conditions such as black foot disease as well as various cancers originating in the lungs, skin, and bladder. In order to efficiently metabolize and excrete arsenic, it is methylated to monomethylarsonic and dimethylarsinic acid. One single enzyme, arsenic methyltransferase (AS3MT) is responsible for generating both metabolites. AS3MT has been purified from several mammalian and nonmammalian species, and its mRNA sequences were determined from amino acid sequences. With the advent of genome technology, mRNA sequences of AS3MT have been predicted from many species throughout the animal kingdom. Horizontal gene transfer had been postulated for this gene through phylogenetic studies, which suggests the importance of this gene in appropriately handling arsenic exposures in various organisms. An altered ability to methylate arsenic is dependent on specific single nucleotide polymorphisms (SNPs) in AS3MT. Reduced AS3MT activity resulting in poor metabolism of iAs has been shown to reduce expression of the tumor suppressor gene, p16, which is a potential pathway in arsenic carcinogenesis. Arsenic is also known to induce oxidative stress in cells. However, the presence of antioxidant response elements (AREs) in the promoter sequences of AS3MT in several species does not correlate with the ability to methylate arsenic. ARE elements are known to bind NRF2 and induce antioxidant enzymes to combat oxidative stress. NRF2 may be partly responsible for the biotransformation of iAs and the generation of methylated arsenic species via AS3MT. In this article, arsenic metabolism, excretion, and toxicity, a discussion of the AS3MT gene and its evolutionary history, and DNA methylation resulting from arsenic exposure have been reviewed.



2010 ◽  
Vol 82 (2) ◽  
pp. 373-381 ◽  
Author(s):  
Kevin A. Francesconi

The presence of arsenic in marine samples was first reported over 100 years ago, and shortly thereafter it was shown that common seafood such as fish, crustaceans, and molluscs contained arsenic at exceedingly high concentrations. It was noted at the time that this seafood arsenic was probably present as an organically bound species because the concentrations were so high that if the arsenic had been present as an inorganic species it would certainly have been toxic to the humans consuming seafood. Investigations in the late 1970s identified the major form of seafood arsenic as arsenobetaine [(CH3)3As+CH2COO–], a harmless organoarsenic compound which, following ingestion by humans, is rapidly excreted in the urine. Since that work, however, over 50 additional arsenic species have been identified in marine organisms, including many important food products. For most of these arsenic compounds, the human toxicology remains unknown. The current status of arsenic in seafood will be discussed in terms of the possible origin of these compounds and the implications of their presence in our foods.



2009 ◽  
Vol 6 (3) ◽  
pp. 226 ◽  
Author(s):  
Somkiat Khokiattiwong ◽  
Narumol Kornkanitnan ◽  
Walter Goessler ◽  
Sabine Kokarnig ◽  
Kevin A. Francesconi

Environmental context. Despite the widespread occurrence of arsenobetaine in marine animals the origin of this arsenic compound remains unknown. A current hypothesis is that arsenobetaine is formed from more complex arsenic compounds found in marine algae. To test this hypothesis, we examined the arsenic compounds in a mangrove ecosystem where algae play a limited role in primary productivity. Abstract. Marine algae are known to bioaccumulate arsenic and transform it into arsenosugars, which are thought to be precursors of the major arsenic compound, arsenobetaine, found in marine animals. Marine ecosystems based on mangrove forests have high nutrient input from mangrove leaves, and thus provide a unique opportunity to study the cycling of arsenic in a marine system where algae are not the dominant food source. Two mangrove forests in Phuket, Thailand were selected as sampling sites for this study. For comparison, samples were also collected from two coral reef sites at and near Phuket. The samples collected included mangrove leaves, corals, algae, molluscs, fish and crustaceans. Arsenic contents in the samples and in aqueous extracts of the samples were determined by hydride generation atomic absorption spectrometry following a dry-ashing mineralisation procedure, and arsenic species were determined in the aqueous extracts by HPLC-MS (mainly ICPMS). Mangrove leaves contained only low concentrations of total arsenic (0.10–0.73 mg kg–1 dry mass) and the aqueous extracts thereof contained inorganic arsenic species, methylarsonate and dimethylarsinate, but arsenosugars were not detected. The total mean arsenic contents (3.2–86 mg kg–1 dry mass) of the animals from the mangrove ecosystem, however, were typical of those found in animal samples from other marine ecosystems. Similarly the arsenic compounds present were typical of those in animals from other marine ecosystems comprising mainly arsenobetaine with smaller quantities of other common arsenicals including arsenosugars, arsenocholine, tetramethylarsonium ion, trimethylarsine oxide and dimethylarsinate. A trimethylated arsenosugar, which is not commonly reported in marine organisms, was a significant arsenical (6–8% of total As) in some gastropod species from the mangrove ecosystem. The coral samples contained mainly arsenosugars and arsenobetaine, and the other animals collected from the coral ecosystem contained essentially the same pattern of arsenicals found for the mangrove animals. The data suggest that food chains based on algae are not necessary for animals to accumulate large concentrations of arsenobetaine.



2012 ◽  
Vol 9 (1) ◽  
pp. 77 ◽  
Author(s):  
A. Price ◽  
W. Maher ◽  
J. Kirby ◽  
F. Krikowa ◽  
E. Duncan ◽  
...  

Environmental contextAlthough arsenic occurs at high concentrations in many marine systems, the influencing factors are poorly understood. The arsenic content of sediments, detritus, suspended particles and organisms have been investigated from different trophic levels in an open seagrass ecosystem. Total arsenic concentrations and arsenic species were organism-specific and determined by a variety of factors including exposure, diet and the organism physiology. AbstractThe distribution and speciation of arsenic within an open marine seagrass ecosystem in Lake Macquarie, NSW, Australia is described. Twenty-six estuarine species were collected from five trophic groups (autotrophs, suspension-feeders, herbivores, detritivores and omnivores, and carnivores). Sediment, detritus, epibiota and micro-invertebrates were also collected and were classified as arsenic source samples. There were no significant differences in arsenic concentrations between trophic groups and between pelagic and benthic feeders. Benthic-dwelling species generally contained higher arsenic concentrations than pelagic-dwelling species. Sediments, seagrass blades and detritus contained mostly inorganic arsenic (50–90 %) and arsenoribosides (10–26 %), with some methylarsonate (9.4–14.6 %) and dimethyarsinate (7.9–9.7 %) in seagrass blades and detritus. Macroalgae contained mostly arsenoribosides (40–100 %). Epibiota and other animals contained predominately arsenobetaine (63–100 %) and varying amounts of dimethyarsinate (0–26 %), monomethyarsonate (0–14.6 %), inorganic arsenic (0–2 %), trimethylarsenic oxide (0–6.6 %), arsenocholine (0–12 %) and tetramethylarsonium ion (0–4.5 %). It was concluded that arsenic concentrations and species within the organisms of the Lake Macquarie ecosystem are species-specific and determined by a variety of factors including exposure, diet and the physiology of the organisms.



2005 ◽  
Vol 2 (2) ◽  
pp. 108 ◽  
Author(s):  
Joel Waring ◽  
William Maher ◽  
Simon Foster ◽  
Frank Krikowa

Environmental Context. In well-oxygenated water and sediments, nearly all arsenic is present as arsenate (AsO43−). As arsenate is a phosphate (PO43−) analogue, organisms living in arsenate-rich environments must acquire the nutrient phosphorus yet avoid arsenic toxicity. Organisms take in and transform arsenic compounds by many means. Three major modes of arsenic biotransformation have been found to occur in the environment—redox transformation between arsenate and arsenite (AsO2−), the reduction and methylation of arsenic, and the biosynthesis of organoarsenic compounds such as arsenobetaine. These biotransformations lead to biogeochemical cycling of arsenic compounds and bioconcentration of arsenic in aquatic organisms and thence into the food web. Abstract. The paper reports the whole-tissue total arsenic concentrations and water-soluble arsenic species in eight common coastal Australian polychaete species. Laboratory experiments showed the period of depuration did not significantly alter the whole-tissue total arsenic concentrations in the two estuarine polychaete species tested. Significant differences were found between the whole-tissue total arsenic concentrations of the eight polychaete species (mean arsenic concentrations ranged from 18 to 101 µg g−1 dry mass). Total arsenic concentrations in polychaete species, grouped on the basis of a combination of their feeding guild and habitat type, were also significantly different with a significant interaction between these factors indicating that both factors simultaneously influence arsenic concentration in polychaetes. A large number of polychaete species contained similar arsenic species with high proportions of arsenobetaine (AB; 57–88%) and relatively low proportions of As3+, As5+, methyarsonic acid, dimethylarsinic acid, arsenocholine, trimethylarsoniopropionate, and tetramethylarsonium ion (not detected to 12%). All polychaete species contained arsenoribosides (5–30%). This study identified two Australian polychaete species with particularly unusual whole-tissue water-soluble arsenic species proportions: Australonuphis parateres contained a very high proportion of trimethylarsoniopropionate (~33%), while Notomastus estuarius had a very low proportion of arsenobetaine (9%) and high proportions of As3+ (~30%), As5+ (~8%), arsenoribosides (30%), and an unknown anionic arsenic species (~4%). Most polychaetes accumulate arsenobetaine, except deposit feeders inhabiting estuarine mud habitats. Thus most polychaetes, which are prey for higher organisms, are a source of arsenobetaine in benthic food webs. Deposit feeders inhabiting estuarine muddy substrates contain appreciable quantities of inorganic arsenic and arsenoribosides that may be metabolized to different end products in higher organisms.



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