Global Metabolomic Characterizations of Microcystis spp. Highlights Clonal Diversity in Natural Bloom-Forming Populations and Expands Metabolite Structural Diversity.

Séverine Le Manach,Marc Edery,Arnaud Catherine,Cécile Bernard,Chakib Djediat,Arul Marie,Benjamin Marie,Charlotte Duval

doi:10.3389/fmicb.2019.00791

Abstract

Cyanobacteria are photosynthetic prokaryotes capable of synthesizing a large variety of secondary metabolites that exhibit significant bioactivity or toxicity. Microcystis constitutes one of the most common cyanobacterial genera, forming the intensive blooms that nowadays arise in freshwater ecosystems worldwide. Species in this genus can produce numerous cyanotoxins (i.e., toxic cyanobacterial metabolites), which can be harmful to human health and aquatic organisms. To better understand variations in cyanotoxin production between clones of Microcystis species, we investigated the diversity of 24 strains isolated from the same blooms or from different populations in various geographical areas. Strains were compared by genotyping with 16S-ITS fragment sequencing and metabolite chemotyping using LC ESI-qTOF mass spectrometry. While genotyping can help to discriminate among different species, the global metabolome analysis revealed clearly discriminating molecular profiles among strains. These profiles could be clustered primarily according to their global metabolite content, then according to their genotype, and finally according to their sampling location. A global molecular network of all metabolites produced by Microcystis species highlights the production of a wide set of chemically diverse metabolites, including a few microcystins, many aeruginosins, microginins, cyanopeptolins, and anabaenopeptins, together with a large set of unknown molecules. These components, which constitute the molecular biodiversity of Microcystis species, still need to be investigated in terms of their structure and potential bioactivites (e.g., toxicity).

Highlights

During recent decades, the frequency and the intensity of cyanobacteria proliferation occurring in continental aquatic ecosystems have increased due to climate and anthropogenic changes (Carey et al, 2012; Sukenik et al, 2015; Paerl, 2018)
In order to better understand the differences in metabolite production between clones of various bloom-forming cyanobacteria from different localities, we investigated here the clonal diversity of 24 Microcystis strains, originating from various geographical areas, using an innovative approach based on global molecular networking
Additional non-metric multidimensional scaling and PERMANOVA analyses based on BrayCurtis index indicated that the ability to produce MC seems to be the first main driver of the global metabolome of Microcystis

Summary

Introduction

The frequency and the intensity of cyanobacteria proliferation occurring in continental aquatic ecosystems have increased due to climate and anthropogenic changes (Carey et al, 2012; Sukenik et al, 2015; Paerl, 2018). Various cyanobacterial genera can synthetize a wide range of secondary metabolites (Welker et al, 2012; Shih et al, 2013), with noticeable bioactivity and high toxicity, causing potential harm to human and aquatic organism populations (Codd et al, 2005; Pearson et al, 2010). These metabolites are believed to affect the proliferative capability of the cyanobacteria themselves (Guljamow et al, 2017). Microcystis species can even overwinter in the benthos, rise from the epilimnion during the summer and can accumulate to form intensive blooms and even scums on the surface (Harke et al, 2016)

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Conclusion