Cyanobacterial Allelochemicals But Not Cyanobacterial Cells Markedly Reduce Microbial Community Diversity.

Filipa Dias,Vitor Vasconcelos,Jorge T Antunes,Pedro N Leão,Tiago Ribeiro,Joana Azevedo

doi:10.3389/fmicb.2017.01495

Abstract

The freshwater cyanobacterium Phormidium sp. LEGE 05292 produces allelochemicals, including the cyclic depsipeptides portoamides, that influence the growth of heterotrophic bacteria, cyanobacteria, and eukaryotic algae. Using 16S rRNA gene amplicon metagenomics, we show here that, under laboratory conditions, the mixture of metabolites exuded by Phormidium sp. LEGE 05292 markedly reduces the diversity of a natural planktonic microbial community. Exposure of the same community to the portoamides alone resulted in a similar outcome. In both cases, after 16 days, alpha-diversity estimates for the allelochemical-exposed communities were less than half of those for the control communities. Photosynthetic organisms, but also different heterotrophic-bacteria taxa were found to be negatively impacted by the allelochemicals. Intriguingly, when Phormidium sp. LEGE 05292 was co-cultured with the microbial community, the latter remained stable and closer to non-exposed than to allelochemical-exposed communities. Overall, our observations indicate that although under optimal growth conditions Phormidium sp. LEGE 05292 is able to synthesize potent allelochemicals that severely impact different microorganisms, its allelopathic effect is not pronounced when in contact with a complex microbial community. Therefore, under ecologically relevant conditions, the allelopathic behavior of this cyanobacterium may be regulated by nutrient availability or by interactions with the surrounding microbiota.

Highlights

The shaping and dynamics of aquatic microbial communities is dependent on several abiotic and biotic factors (Fuhrman, 2009; Yu et al, 2014)
LEGE 05292 (Leão et al, 2009a, 2010) – were maintained in Z8 medium (Kotai, 1972), at 25◦C and under a 14:10 h light (∼30 μmol photons m−2 s−1)/dark cycle. This unicyanobacterial culture has not been determined to be axenic, but no contamination is visible in exponentially growing cultures by light microscopy under high magnification, probably due to the antibiotic properties that have been attributed to the portoamides
Comparison of the two spectra indicated that portoamides A and B were not main components of the extract

Summary

Introduction

The shaping and dynamics of aquatic microbial communities is dependent on several abiotic (e.g., nutrient levels, salinity, light quality and quantity, mixing) and biotic (e.g., grazing, competition, cell–cell contact, viruses) factors (Fuhrman, 2009; Yu et al, 2014). Two types of studies (physically separated co-cultures and/or filtrate addition) using typically one producing (allelopathic) and one target (sensitive) organism have contributed to the bulk of the literature on aquatic allelopathy (Legrand et al, 2003; Leão et al, 2009b). These experimental approaches allow control over other ecological phenomena such as cell–cell interactions or nutrient competition. The advent of affordable, highthroughput sequencing technologies has created an opportunity for experimentally interrogating chemically mediated biotic interactions in complex communities These technologies have enabled investigations of the role of natural small-molecules in the gut microbiota (e.g., Thompson et al, 2015)

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Results