microorganisms Review Reviewing Interspecies Interactions as a Driving Force Affecting the Community Structure in Lakes via Cyanotoxins Azam Omidi 1 , Stephan Pflugmacher 2, Aaron Kaplan 3 , Young Jun Kim 4 and Maranda Esterhuizen 4,5,6,* 1 Chair Ecological Impact Research and Ecotoxicology, Technische Universität Berlin, 10587 Berlin, Germany; [email protected] 2 Clayton H. Riddell Faculty of Environment, Earth, and Resources, University of Manitoba, Wallace Bldg., 125 Dysart Rd, Winnipeg, MB R3T 2N2, Canada; Stephan.Pfl[email protected] 3 Department of Plant and Environmental Sciences, Edmond J. Safra Campus, The Hebrew University of Jerusalem, Jerusalem 9190401, Israel; [email protected] 4 Joint Laboratory of Applied Ecotoxicology, Korean Institute of Science and Technology Europe (KIST), Campus 7.1, 66123 Saarbrücken, Germany; [email protected] 5 Ecosystems and Environment Research Programme, Faculty of Biological and Environmental Sciences, University of Helsinki, Niemenkatu 73, 15140 Lahti, Finland 6 Finland and Helsinki Institute of Sustainability Science (HELSUS), Fabianinkatu 33, 00014 Helsinki, Finland * Correspondence: maranda.esterhuizen@helsinki.fi Abstract: The escalating occurrence of toxic cyanobacterial blooms worldwide is a matter of con- cern. Global warming and eutrophication play a major role in the regularity of cyanobacterial blooms, which has noticeably shifted towards the predomination of toxic populations. Therefore, understanding the effects of cyanobacterial toxins in aquatic ecosystems and their advantages to the producers are of growing interest. In this paper, the current literature is critically reviewed to provide further insights into the ecological contribution of cyanotoxins in the variation of the lake Citation: Omidi, A.; Pflugmacher, S.; community diversity and structure through interspecies interplay. The most commonly detected and Kaplan, A.; Kim, Y.J.; Esterhuizen, M. studied cyanobacterial toxins, namely the microcystins, anatoxins, saxitoxins, cylindrospermopsins Reviewing Interspecies Interactions β as a Driving Force Affecting the and -N-methylamino-L-alanine, and their ecotoxicity on various trophic levels are discussed. This Community Structure in Lakes via work addresses the environmental characterization of pure toxins, toxin-containing crude extracts Cyanotoxins. Microorganisms 2021, 9, and filtrates of single and mixed cultures in interspecies interactions by inducing different physi- 1583. https://doi.org/10.3390/ ological and metabolic responses. More data on these interactions under natural conditions and microorganisms9081583 laboratory-based studies using direct co-cultivation approaches will provide more substantial infor- mation on the consequences of cyanotoxins in the natural ecosystem. This review is beneficial for Academic Editor: Ulrich (Uli) Stingl understanding cyanotoxin-mediated interspecies interactions, developing bloom mitigation tech- nologies and robustly assessing the hazards posed by toxin-producing cyanobacteria to humans and Received: 1 July 2021 other organisms. Accepted: 23 July 2021 Published: 25 July 2021 Keywords: cyanobacteria; cyanotoxins; interspecies interactions; allelopathy; lake ecosystems Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affil- 1. Introduction iations. In aquatic ecosystems, the primary producers, such as cyanobacteria, algae, bacteria and plants, often function as foundation as well as keystone species [1] because they drive primary production, play a pivotal role in food webs and nutrient cycling and create habi- tats for other species. Several factors can influence the structure and biodiversity over time Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. within a community, such as abiotic and biotic parameters, frequency, level of disturbances, This article is an open access article chance events and the interactions between species, including via allelopathy [2–6]. distributed under the terms and Species in a community may interact with each other in various ways, forming a conditions of the Creative Commons biocoenosis. The interactions can be interspecies or intraspecies, having a strong influence Attribution (CC BY) license (https:// on the evolution of the species, and often the partners coevolve [7]. Traditionally, these creativecommons.org/licenses/by/ interactions have been classified and termed as follows (Figure1): Neutralism (0/0), 4.0/). mutualism (+/+), Competition (-/-), Commensalism (+/0), Amensalism (-/0), parasitism Microorganisms 2021, 9, 1583. https://doi.org/10.3390/microorganisms9081583 https://www.mdpi.com/journal/microorganisms Microorganisms 2021, 9, x FOR PEER REVIEW 2 of 26 Microorganisms 2021, 9, 1583 2 of 25 interactions have been classified and termed as follows (Figure 1): Neutralism (0/0), mu- tualism (+/+), Competition (-/-), Commensalism (+/0), Amensalism (-/0), parasitism (+/-) and Predation (+/-) [8,9]. These interactions, both as inter- and intraspecies exchanges, (+/-) and Predation (+/-) [8,9]. These interactions, both as inter- and intraspecies exchanges, change with both time and location and are dynamic based on the prevailing conditions change with both time and location and are dynamic based on the prevailing conditions being either beneficial, inhibitory or commensal [10,11]. being either beneficial, inhibitory or commensal [10,11]. Figure 1. Long-terms interspecies interactions. Lines indicate how each species is influenced by the Figure 1. Long-terms interspecies interactions. Lines indicate how each species is influenced by the other.other. Cyanobacteria frequently form blooms and dominate the aquatic ecosystem commu- Cyanobacteria frequently form blooms and dominate the aquatic ecosystem commu- nity. These blooms influence water quality through the sheer quantity of cyanobacterial nity. These blooms influence water quality through the sheer quantity of cyanobacterial cells and the release of secondary metabolites, including toxic compounds, thereby affecting cells and the release of secondary metabolites, including toxic compounds, thereby affect- the rest of the biological community and their ecosystem functions and services [12,13]. The ing the rest of the biological community and their ecosystem functions and services frequency and prevalence of blooms are increasing, likely due to anthropogenic effects [14], [12,13]. The frequency and prevalence of blooms are increasing, likely due to anthropo- leading to excess nutrients and global warming [15]. Interestingly, there are indeed coex- genic effects [14], leading to excess nutrients and global warming [15]. Interestingly, there isting antagonists in these environments where blooms occur, such as cyanolytic bacteria are indeed coexisting antagonists in these environments where blooms occur, such as cy- and grazers [16–18]. Regardless, cyanobacterial blooms annually arise globally [19], of- anolytic bacteria and grazers [16–18]. Regardless, cyanobacterial blooms annually arise ten in succession with green algae and diatoms [20–22]. It is essential to recognize that glconditionsobally [19] associated, often in succession with blooms with may green lead algae to reduced and diatoms competition [20–22 or]. predationIt is essential on theto recognizetaxa forming that theconditions blooms associated [15]. However, with blooms the exact may mechanism lead to reduced used to competition achieve dominance or pre- dationand the on interactions the taxa forming involved the are blooms poorly understood.[15]. However, Allelopathic the exact interactions mechanism could used cause to achievecyanobacterial dominance dominance and the interactions as allelochemicals involved could are poorly allow cyanobacteriaunderstood. Allelopathic to outcompete in- teractionsother phytoplankton. could cause Ascyanobacterial the frequency dominance of cyanobacterial as allelochemicals blooms is increasing could allow worldwide, cyano- bacteriatheir allelopathic to outcompete effects other on other phytoplankton. aquatic organisms As the arefrequency attracting of growingcyanobacterial attention. blooms Con- issidering increasing the worldwide, major societal their and allelopathic economic impactseffects on of other cyanobacterial aquatic organisms blooms, informationare attract- ingregarding growing allelopathic attention. Considering interspecies the interactions major societal could and also economic be vital in impacts developing of cyanobac- methods terialto control blooms, blooms information development. regarding allelopathic interspecies interactions could also be vital inOver developing the past methods decades, to more control than blooms 2000 cyanobacterialdevelopment. secondary metabolites have beenOver reported the past [23 ].decades, Previous more studies than suggested 2000 cyanobacterial the involvement secondary of the metabolites other secondary have beenmetabolites reported rather [23]. thanPrevious or along studies with suggested cyanotoxins the ininvolvement the allelopathic of th effectse other [ 24secondary,25]. Two metaboliteswell-characterized rather than allelochemicals, or along with fischerellin cyanotoxins produced in the allelopathic by Fischerella effects muscicola [24,25[26]. Two] and wellcyanobacterin-characterized produced allelochemicals, by Scytonema fischerellin hofmanni produced[27], have by beenFischerella implicated muscicola in photosyn- [26] and cyanobacterinthesis inhibition produced of co-occurring