Identification of genes for anatoxin-a biosynthesis in Cuspidothrix issatschenkoi

Jiang, Yongguang; Song, Gaofei; Pan, Qianqian; Yang, Yiming; Li, Renhui

doi:10.1016/j.hal.2015.05.005

Cited by 25 publications

(23 citation statements)

References 55 publications

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“…All anatoxin-a gene annotations from these sequences matched those previously reported (Rantala-Ylinen et al, 2011;Méjean et al, 2014;Jiang et al, 2015;Brown et al, 2016). The arrangement of the anaB-G genes was similar to the three reference operons ( Figure 4A).…”

Section: Anatoxin-asupporting

confidence: 81%

Microbial diversity and metabolic potential in cyanotoxin producing cyanobacterial mats throughout a river network

Bouma‐Gregson

Olm

Probst

et al. 2018

Preprint

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Microbial mats formed by Cyanobacteria of the genus Phormidium produce the neurotoxin anatoxin-a that has been linked to animal deaths. Blooms of planktonic Cyanobacteria have long been of concern in lakes, but recognition of potential harmful impacts of riverine benthic cyanobacterial mats is more recent. Consequently little is known about the diversity of the biosynthetic capacities of cyanobacterial species and associated microbes in mats throughout river networks. Here we performed metagenomic sequencing for 22 Phormidium-dominated microbial mats collected across the Eel River network in Northern California to investigate cyanobacterial and co-occurring microbial assemblage diversity, probe their metabolic potential and evaluate their capacities for toxin production. We genomically defined four Cyanobacterial species clusters that occur throughout the river network, three of which have not been described previously. From the genomes of seven strains from one species group we describe the first anatoxin-a operon from the genus Phormidium. Community composition within the mat appears to be associated with the presence of Cyanobacteria capable of producing anatoxin-a. Bacteroidetes, Proteobacteria, and novel Verrucomicrobia dominated the microbial assemblages. Interestingly, some mats also contained organisms from candidate phyla such as Canditatus Kapabacteria, as well as Absconditabacteria (SR1), Parcubacteria (OD1) and Peregrinibacteria (PER) within the Candidate Phyla Radiation. Oxygenic photosynthesis and carbon respiration were the most common metabolisms detected in mats but other metabolic capacities include aerobic anoxygenic photosynthesis, sulfur compound oxidation and breakdown of urea. The results reveal the diversity of metabolisms fueling the growth of mats, and a relationship between microbial assemblage composition and the distribution of anatoxin-a producing cyanobacteria within freshwater Phormidium mats in river networks.

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Section: Anatoxin-asupporting

confidence: 81%

Microbial diversity and metabolic potential in cyanotoxin producing cyanobacterial mats throughout a river network

Bouma‐Gregson

Olm

Probst

et al. 2018

Preprint

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“…PCC 6407, a very close relative of Oscillatoria sp. PCC 6506 producing homoanatoxin-a, 20,21 in two closely related Cuspidothrix issatschenkoi strains producing homoanatoxin-a, 22 and in Cylindrospermum stagnale PCC 7417. 20 Interestingly, a gene that we named anaK (Figure 1), coding for a putative F 420 -dependent oxido-reductase, has been identified in the C. stagnale PCC 7417 ana cluster of genes, and we noted in a preliminary investigation that C. stagnale PCC 7417 produced dihydroanatoxin-a.…”

Section: * S Supporting Informationmentioning

confidence: 99%

Dihydroanatoxin-a Is Biosynthesized from Proline in Cylindrospermum stagnale PCC 7417: Isotopic Incorporation Experiments and Mass Spectrometry Analysis

et al. 2016

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LC-MS and GC-MS analytical conditions have been developed to detect the cis- and trans-epimers (relative configuration of the carbon bearing the acetyl or propionyl group) of dihydroanatoxin-a and dihydrohomoanatoxin-a, in biological samples. These compounds epimerize under acidic conditions, yielding a major species that was tentatively assigned as the cis-epimer. Cylindrospermum stagnale PCC 7417 was definitively shown to produce dihydroanatoxin-a (1.2 mg/g dried cells). Oscillatoria sp. PCC 9107, Oscillatoria sp. PCC 6506, and C. stagnale PCC 7417, which produce anatoxin-a, homoanatoxin-a, and dihydroanatoxin-a, respectively, were cultivated in the presence of isotopically labeled proline, and the toxins were extracted. Interpretation of the GC-MS electron ionization mass spectra of these labeled anatoxins showed that they are all biosynthesized from proline and that the positions of the labels in these molecules are identical. These data and the fact that the ana cluster of genes is conserved in these cyanobacteria suggest that dihydroanatoxin-a is formed by the reduction of either anatoxin-a or its precursor in a specific step involving AnaK, an F420-dependent oxido-reductase whose gene is found in the ana gene cluster in C. stagnale PCC 7417. This is the first report of a cyanobacterium producing dihydroanatoxin-a, suggesting that other producers are present in the environment.

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“…In that study, the authors also reported that dihydroanatoxin‐a concentrations decreased when N and P concentrations were elevated (21 mg l −1 and 3 mg l −1 respectively), whereas homoanatoxin‐a quota increased when P concentrations were reduced below 0.08 mg l −1 . Potentially complicating the identification of environmental drivers was the observation of transcripts from several ana genes but an absence of detectable toxin in Cuspidothrix (formerly Aphanizomenon ) issatschenkoi CHABD3 (Jiang et al ., ); this raised the possibility that anatoxin‐a synthesis may be subject to post‐transcriptional regulation.…”

Section: Overview Of Cyanotoxins and Their Putative Environmental Drimentioning

confidence: 99%

Moving towards adaptive management of cyanotoxin‐impaired water bodies

Paerl

Otten

Joyner

2016

Microbial Biotechnology

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SummaryThe cyanobacteria are a phylum of bacteria that have played a key role in shaping the Earth's biosphere due to their pioneering ability to perform oxygenic photosynthesis. Throughout their history, cyanobacteria have experienced major biogeochemical changes accompanying Earth's geochemical evolution over the past 2.5+ billion years, including periods of extreme climatic change, hydrologic, nutrient and radiation stress. Today, they remain remarkably successful, exploiting human nutrient over‐enrichment as nuisance “blooms.” Cyanobacteria produce an array of unique metabolites, the functions and biotic ramifications of which are the subject of diverse ecophysiological studies. These metabolites are relevant from organismal and ecosystem function perspectives because some can be toxic and fatal to diverse biota, including zooplankton and fish consumers of algal biomass, and high‐level consumers of aquatic food sources and drinking water, including humans. Given the long history of environmental extremes and selection pressures that cyanobacteria have experienced, it is likely that that these toxins serve ecophysiological functions aimed at optimizing growth and fitness during periods of environmental stress. Here, we explore the molecular and ecophysiological mechanisms underlying cyanotoxin production, with emphasis on key environmental conditions potentially controlling toxin production. Based on this information, we offer potential management strategies for reducing cyanotoxin potentials in natural waters; for cyanotoxins with no clear drivers yet elucidated, we highlight the data gaps and research questions that are still lacking. We focus on the four major classes of toxins (anatoxins, cylindrospermopsins, microcystins and saxitoxins) that have thus far been identified as relevant from environmental health perspectives, but caution there may be other harmful metabolites waiting to be elucidated.

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Identification of genes for anatoxin-a biosynthesis in Cuspidothrix issatschenkoi

Cited by 25 publications

References 55 publications

Microbial diversity and metabolic potential in cyanotoxin producing cyanobacterial mats throughout a river network

Microbial diversity and metabolic potential in cyanotoxin producing cyanobacterial mats throughout a river network

Dihydroanatoxin-a Is Biosynthesized from Proline in Cylindrospermum stagnale PCC 7417: Isotopic Incorporation Experiments and Mass Spectrometry Analysis

Moving towards adaptive management of cyanotoxin‐impaired water bodies

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