Woronichinia naegeliana: A common nontoxigenic component of temperate freshwater cyanobacterial blooms with 30% of its genome in transposons

•The complete genome of Woronichinia naegeliana WA131 was determined from a microcystin-containing CyanoHAB in a US Pacific NW freshwater lake (2018).•The larger genome size of 7.9 Mpb, compared to other bloom-forming cyanobacteria, is mostly attributable to insertion elements and their transposase genes, which are often present in high copy number. Pseudogenes are also relatively abundant, but most of these are transposases.•The genome contains no genes for cyanotoxins or the common taste-and-odor compounds. Gene clusters for the production of anabaenopeptins, cyanopeptolins, microginins and some post-translationally modified peptides are present.•The genome of this planktonic, non-diazotrophic cyanobacterium contains genes commonly found in other bloom-forming cyanobacteria, but surprisingly lacks genes for nitrite and nitrate reductases, making this cyanobacterium dependent on reduced and organic forms of nitrogen.•In the US Pacific NW, Woronichinia naegeliana was a common component of freshwater HABs across the period 2007–2019, often being the dominant or subdominant cyanobacterium. Monitoring in the U.S. state of Washington across the period 2007–2019 showed that Woronichinia has been present in many lakes state-wide. This cyanobacterium was commonly dominant or sub-dominant in cyanobacterial blooms in the wet temperate region west of the Cascade Mountains. In these lakes, Woronichinia often co-existed with Microcystis, Dolichospermum and Aphanizomenon flos-aquae and the cyanotoxin microcystin has often been present in those blooms, although it has not been known whether Woronichinia is a toxin producer. We report the first complete genome of Woronichinia naegeliana WA131, assembled from the metagenome of a sample collected from Wiser Lake, Washington, in 2018. The genome contains no genes for cyanotoxin biosynthesis or taste-and-odor compounds, but there are biosynthetic gene clusters for other bioactive peptides, including anabaenopeptins, cyanopeptolins, microginins and ribosomally produced, post-translationally modified peptides. Genes for photosynthesis, nutrient acquisition, vitamin synthesis and buoyancy that are typical of bloom-forming cyanobacteria are present, although nitrate and nitrite reductase genes are conspicuously absent. However, the 7.9 Mbp genome is 3–4 Mbp larger than those of the above-mentioned frequently co-existing cyanobacteria. The increased genome size is largely due to an extraordinary number of insertion sequence eleme