Vol.:(0123456789) 1 3
Journal of Chemical Ecology
https://doi.org/10.1007/s10886-021-01315-5
Grazer‑Induced Chemical Defense in a Microcystin‑Producing
Microcystis aeruginosa (Cyanobacteria) Exposed to Daphnia gessneri
Infochemicals
Mauro Cesar Palmeira Vilar
1
· Thiago Ferreira da Costa Pena Rodrigues
1
· Aloysio da Silva Ferrão‑Filho
2
·
Sandra Maria Feliciano de Oliveira e Azevedo
1
Received: 28 July 2021 / Revised: 9 September 2021 / Accepted: 14 September 2021
© The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature 2021
Abstract
Cyanobacteria are photosynthetic microorganisms that compose phytoplankton and therefore have a trophic relationship
with zooplankton, which represent an important link for energy fux in aquatic food webs. Several species can form blooms
and produce bioactive metabolites known as cyanotoxins. However, the ecological and adaptative role of these toxins are
still under debate. Many studies have addressed the cyanotoxins’ function in defense against herbivory when grazing pres-
sure by zooplankton plays a role in phytoplankton top-down control. Thus, the present study evaluated the ecophysiological
responses of the cyanobacterial strain Microcystis aeruginosa NPLJ-4 underlying the chemical induced defense against
the cladoceran Daphnia gessneri. Exposure to predator infochemicals consisted of cultures established in ASM-1 medium
prepared in a fltrate from a culture of adults of D. gessneri at an environmentally relevant density. Daphnia infochemicals
promoted a signifcant increase in toxin production by M. aeruginosa. However, no diferences in growth were observed,
despite a signifcant increase in both maximum photosynthetic efciency and electron transport rate in response to zooplank-
ton. Additionally, there was no signifcant variation in the production of exopolysaccharides. Overall, although a grazer-
induced defense response was demonstrated, there were no efects on M. aeruginosa ftness, which maintained its growth in
the presence of Daphnia alarm cues.
Keywords Zooplankton · Kairomone · Microcystins · Cyanobacteria · Predator–prey
Introduction
Cyanobacteria naturally occur in the phytoplankton
community, contributing to primary production and
comprising part of the zooplankton diet in aquatic food
webs (Moustaka-Gouni and Sommer 2020). However,
several cyanobacterial genera produce a range of bioactive
secondary metabolites, which can impact zooplankton
survivorship and reproduction (Esterhuizen-Londt et al.
2016; Ferrão-Filho and Kozlowsky-Suzuki 2011; Ferrão-
Filho et al. 2019; Nandini et al. 2017) and even swimming
and feeding behavior (Bownik 2016, 2017; Ferrão-Filho
et al. 2020; Ferrão-Filho et al. 2014,), thereby limiting its
role in phytoplankton top-down control.
Among toxic cyanobacteria, Microcystis is a worldwide
distributed genus that has been reported to form dense
blooms and produce toxic peptides, such as microcyst-
ins (MCs) and other cyanopeptides (Harke et al. 2016;
Huang and Zimba 2019). MCs are chemically charac-
terized as cyclic heptapeptides and classifed according
to their action mechanism as potent inhibitors of phos-
phatases protein 1 and 2A (Carmichael et al. 2001). Up to
date more than 270 MC variants are reported according to
structural variations resulted from frequent substitutions
and demethylations in amino acids at positions 2 and 4,
Thiago Ferreira da Costa Pena Rodrigues have contributed equally
to this study.
* Mauro Cesar Palmeira Vilar
maurovilar@gmail.com
1
Laboratory of Ecophysiology and Toxicology
of Cyanobacteria, Carlos Chagas Filho Institute
of Biophysics, Federal University of Rio de Janeiro,
Rio de Janeiro 21949-902, Brazil
2
Laboratory of Evaluation and Promotion of Environmental
Health, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro,
RJ 21040-360, Brazil