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

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...

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Main Authors: Elisabeth Entfellner, Ruibao Li, Yiming Jiang, Jinlong Ru, Jochen Blom, Li Deng, Rainer Kurmayer
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-07-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2022.901762/full
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author Elisabeth Entfellner
Ruibao Li
Ruibao Li
Ruibao Li
Yiming Jiang
Jinlong Ru
Jochen Blom
Li Deng
Rainer Kurmayer
author_facet Elisabeth Entfellner
Ruibao Li
Ruibao Li
Ruibao Li
Yiming Jiang
Jinlong Ru
Jochen Blom
Li Deng
Rainer Kurmayer
author_sort Elisabeth Entfellner
collection DOAJ
description 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.
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spelling doaj.art-8e7a54c4439e4658aaa7db93a9b800c92022-12-22T00:58:51ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-07-011310.3389/fmicb.2022.901762901762Toxic/Bioactive Peptide Synthesis Genes Rearranged by Insertion Sequence Elements Among the Bloom-Forming Cyanobacteria PlanktothrixElisabeth Entfellner0Ruibao Li1Ruibao Li2Ruibao Li3Yiming Jiang4Jinlong Ru5Jochen Blom6Li Deng7Rainer Kurmayer8Research Department for Limnology, University of Innsbruck, Mondsee, AustriaResearch Department for Limnology, University of Innsbruck, Mondsee, AustriaInstitute of Virology, Helmholtz Zentrum München, Munich, GermanyDepartment of Ecology and Institute of Hydrobiology, Jinan University, Guangzhou, ChinaInstitute of Virology, Helmholtz Zentrum München, Munich, GermanyInstitute of Virology, Helmholtz Zentrum München, Munich, GermanyBioinformatics and Systems Biology, Justus-Liebig-University, Giessen, GermanyInstitute of Virology, Helmholtz Zentrum München, Munich, GermanyResearch Department for Limnology, University of Innsbruck, Mondsee, AustriaIt 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.https://www.frontiersin.org/articles/10.3389/fmicb.2022.901762/fullharmful algal bloomssecondary metabolitesinsertion sequence elementsmicroevolutionchromosomal rearrangementsgenome size variation
spellingShingle Elisabeth Entfellner
Ruibao Li
Ruibao Li
Ruibao Li
Yiming Jiang
Jinlong Ru
Jochen Blom
Li Deng
Rainer Kurmayer
Toxic/Bioactive Peptide Synthesis Genes Rearranged by Insertion Sequence Elements Among the Bloom-Forming Cyanobacteria Planktothrix
Frontiers in Microbiology
harmful algal blooms
secondary metabolites
insertion sequence elements
microevolution
chromosomal rearrangements
genome size variation
title Toxic/Bioactive Peptide Synthesis Genes Rearranged by Insertion Sequence Elements Among the Bloom-Forming Cyanobacteria Planktothrix
title_full Toxic/Bioactive Peptide Synthesis Genes Rearranged by Insertion Sequence Elements Among the Bloom-Forming Cyanobacteria Planktothrix
title_fullStr Toxic/Bioactive Peptide Synthesis Genes Rearranged by Insertion Sequence Elements Among the Bloom-Forming Cyanobacteria Planktothrix
title_full_unstemmed Toxic/Bioactive Peptide Synthesis Genes Rearranged by Insertion Sequence Elements Among the Bloom-Forming Cyanobacteria Planktothrix
title_short Toxic/Bioactive Peptide Synthesis Genes Rearranged by Insertion Sequence Elements Among the Bloom-Forming Cyanobacteria Planktothrix
title_sort toxic bioactive peptide synthesis genes rearranged by insertion sequence elements among the bloom forming cyanobacteria planktothrix
topic harmful algal blooms
secondary metabolites
insertion sequence elements
microevolution
chromosomal rearrangements
genome size variation
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.901762/full
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