Abstract
ABSTRACTHarmful cyanobacterial bloom occurrences have increased worldwide due to climate change and eutrophication, causing nuisance and animal deaths. Species from the benthic cyanobacterial genus Microcoleus are ubiquitous and form thick mats in freshwater systems, such as rivers, that are sometimes toxic due to the production of potent neurotoxins (anatoxins). Anatoxin-producing (toxic) strains typically coexist with non-anatoxin-producing (nontoxic) strains in mats, although the reason for this is unclear. To determine the genetic mechanisms differentiating toxic and nontoxic Microcoleus, we sequenced and assembled genomes from 11 cultures and compared these to another 31 Microcoleus genomes. Average nucleotide identities (ANI) indicate that toxic and nontoxic strains are distinct species (ANI, <95%), and only 6% of genes are shared across all 42 genomes, suggesting a high level of genetic divergence among Microcoleus strains. Comparative genomics showed substantial genome streamlining in toxic strains and a potential dependency on external sources for thiamine and sucrose. Toxic and nontoxic strains are further differentiated by an additional set of putative nitrate transporter (nitrogen uptake) and cyanophycin (carbon and nitrogen storage) genes, respectively. These genes likely confer distinct competitive advantages based on nutrient availability and suggest nontoxic strains are more robust to nutrient fluctuations. Nontoxic strains also possess twice as many transposable elements, potentially facilitating greater genetic adaptation to environmental changes. Our results offer insights into the divergent evolution of Microcoleus strains and the potential for cooperative and competitive interactions that contribute to the co-occurrence of toxic and nontoxic species within mats.
Highlights
Harmful cyanobacterial bloom occurrences have increased worldwide due to climate change and eutrophication, causing nuisance and animal deaths
Production of anatoxin-a, homoanatoxin-a, or chemical variants of these was confirmed for the 3 isolates with anatoxin gene clusters by liquid chromatography coupled with tandem mass spectrometry (LC-MS/MS) (Table S1)
We compared these to a further 31 metagenome-assembled genomes (MAGs) previously obtained from nonaxenic isolates (3 toxic) and mats sampled from rivers (6 toxic, 22 nontoxic) [8, 19, 30], where the 6 mat-derived MAGs with anatoxin gene clusters were spatially associated with anatoxins [8, 19]
Summary
Harmful cyanobacterial bloom occurrences have increased worldwide due to climate change and eutrophication, causing nuisance and animal deaths. Cyanobacteria first appeared on Earth over two billion years ago and are credited with the evolution of aerobic life [1] Despite this contribution, the increased occurrence of cyanobacterial planktonic blooms and benthic proliferations, due to anthropogenic activity, has severely disrupted aquatic habitats and deteriorated water quality [2]. Some Microcoleus species produce a neurotoxin (anatoxin-a) that has been linked to animal deaths in many countries, including the United States, the Netherlands, New Zealand, Germany, and France [12], and can accumulate in aquatic organisms [13] Both anatoxin-producing and non-anatoxin-producing Microcoleus strains ( referred to as toxic and nontoxic strains, respectively) are often found co-occurring within a single mat (e.g., coating a riverbed cobble), where their relative abundances determine the toxin concentration in the mat [5, 11, 14, 15]. Nontoxic Microcoleus strains are reported to have higher cell concentrations and higher maximum growth rates than toxic strains, regardless of nutrient concentrations (phosphorus and nitrogen), suggesting higher energy costs associated with toxin production [14]
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