Toxic/Bioactive Peptide Synthesis Genes Rearranged by Insertion Sequence Elements Among the Bloom-Forming Cyanobacteria Planktothrix

Elisabeth Entfellner; Ruibao Li; Yiming Jiang; Jinlong Ru; Jochen Blom; Li Deng; Rainer Kurmayer

doi:10.3389/fmicb.2022.901762

Toxic/Bioactive Peptide Synthesis Genes Rearranged by Insertion Sequence Elements Among the Bloom-Forming Cyanobacteria Planktothrix

Front Microbiol. 2022 Jul 28:13:901762. doi: 10.3389/fmicb.2022.901762. eCollection 2022.

Authors

Elisabeth Entfellner¹, Ruibao Li^{1

2

3}, Yiming Jiang², Jinlong Ru², Jochen Blom⁴, Li Deng², Rainer Kurmayer¹

Affiliations

¹ Research Department for Limnology, University of Innsbruck, Mondsee, Austria.
² Institute of Virology, Helmholtz Zentrum München, Munich, Germany.
³ Department of Ecology and Institute of Hydrobiology, Jinan University, Guangzhou, China.
⁴ Bioinformatics and Systems Biology, Justus-Liebig-University, Giessen, Germany.

Abstract

It has been generally hypothesized that mobile elements can induce genomic rearrangements and influence the distribution and functionality of toxic/bioactive peptide synthesis pathways in microbes. In this study, we performed in depth genomic analysis by completing the genomes of 13 phylogenetically diverse strains of the bloom-forming freshwater cyanobacteria Planktothrix spp. to investigate the role of insertion sequence (IS) elements in seven pathways. Chromosome size varied from 4.7-4.8 Mbp (phylogenetic Lineage 1 of P. agardhii/P. rubescens thriving in shallow waterbodies) to 5.4-5.6 Mbp (Lineage 2 of P. agardhii/P. rubescens thriving in deeper physically stratified lakes and reservoirs) and 6.3-6.6 Mbp (Lineage 3, P. pseudagardhii/P. tepida including planktic and benthic ecotypes). Although the variation in chromosome size was positively related to the proportion of IS elements (1.1-3.7% on chromosome), quantitatively, IS elements and other paralogs only had a minor share in chromosome size variation. Thus, the major part of genomic variation must have resulted from gene loss processes (ancestor of Lineages 1 and 2) and horizontal gene transfer (HGT). Six of seven peptide synthesis gene clusters were found located on the chromosome and occurred already in the ancestor of P. agardhii/P. rubescens, and became partly lost during evolution of Lineage 1. In general, no increased IS element frequency in the vicinity of peptide synthesis gene clusters was observed. We found a higher proportion of IS elements in ten breaking regions related to chromosomal rearrangements and a tendency for colocalization of toxic/bioactive peptide synthesis gene clusters on the chromosome.

Keywords: chromosomal rearrangements; cyanotoxins; genome size variation; harmful algal blooms; horizontal gene transfer; insertion sequence elements; microevolution; secondary metabolites.