Benthic Cyanobacterial Diversity and Antagonistic Interactions in Abrolhos Bank: Allelopathy, Susceptibility to Herbivory, and Toxicity

Felipe De Vargas Ribeiro,Taiara Aguiar Caires,Paulo Sergio Salomon,Guilherme Henrique Pereira-Filho,Rodrigo Leão De Moura,Giovana De Oliveira Fistarol,Marcela Alvarenga De Almeida Simões,Alexandre Brauns Cazelgrandi,Paulo Iiboshi Hargreaves,Renato Crespo Pereira,Livia Bonetti Villela

doi:10.3389/fmars.2021.790277

Abstract

Benthic cyanobacterial mats (BCMs) are conspicuous components of coral reef communities, where they play key ecological roles as primary producers among others. BCMs often bloom and might outcompete neighboring benthic organisms, including reef-building corals. We investigated the cyanobacterial species composition of three BCMs morphotypes from the marginal reef complex of Abrolhos Bank (Southeastern Brazil). Also, we assessed their allelopathic effects on coral zooxanthellae, their susceptibility to herbivory by fish, and their toxicity to brine shrimp nauplii. Morphology and 16S rDNA sequencing unveiled the cyanobacteria Moorena bouillonii, Okeania erythroflocculosa, Adonisia turfae, Leptolyngbya sp., and Halomicronema sp. as components of BCMs from Abrolhos. BCMs cell-free filtrates and extracts exerted an allelopathic effect by reducing the growth of the ex hospite Symbiodinium sp. in culture. BCMs-only treatments remained untouched in field susceptibility assays in contrast to macroalgae only and mixed BCMs-macroalgae treatments that had the macroalgae fully removed by reef fish. Crude aqueous extracts from BCMs were toxic to brine shrimps in acute assays. Besides unveiling the diversity of BCMs consortia in Abrolhos, our results cast some light on their allelopathy, antiherbivory, and toxicity properties. These antagonistic interactions might promote adverse cascading effects during benthic cyanobacteria blooms and in gradual shifts to BCMs-dominated states.

Highlights

Benthic cyanobacterial mats (BCMs) are ubiquitous in coral reef ecosystems, where they contribute to critical functions such as nitrogen fixation, sulfate reduction, and primary production (Charpy et al, 2007)
The BCMs were predominantly composed of M. bouillonii or O. erythroflocculosa, non-ramified cyanobacteria species enclosed in exopolysaccharide sheaths and exhibit discoid cells arranged in wide trichomes, corresponding to the Oscillatoriales order (Komárek and Anagnostidis, 2005)
The BCMs from PABBCM presented different macroscopic morphologies and cyanobacteria taxonomic compositions than those collected from PLESBCM

Summary

Introduction

Benthic cyanobacterial mats (BCMs) are ubiquitous in coral reef ecosystems, where they contribute to critical functions such as nitrogen fixation, sulfate reduction, and primary production (Charpy et al, 2007). The term BCMs is used to define a range of cyanobacteria-rich mats that might display diverse morphologies, from periphytic biofilms and horizontally-spreading mats over sediment and rubble, to tufts and fronds of various heights, up to tens of centimeters (Graham and Wilcox, 2000; Charpy et al, 2007; Cissell et al, 2019; Cissell and McCoy, 2021). Filamentous cyanobacteria can be found entangled in other structurally more complex benthic assemblages, namely turf (Connell et al, 2014). These mats can be formed by a single genus (Paul et al, 2005) or by a consortium of multiple taxa (Echenique-Subiabre et al, 2015), including protists and noncyanobacterial, heterotrophic prokaryotes, and viruses (Cissell and McCoy, 2021). Dapis Engene et al (2018)] and several new species within the Lyngbya complex (Engene et al, 2012, 2013b, 2018; Tronholm and Engene, 2019)

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