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Tiny Microbes with a Big Impact: the Role of Cyanobacteria and Their Metabolites in Shaping Our Future

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Tiny Microbes with a Big Impact: the Role of Cyanobacteria and Their Metabolites in Shaping Our Future marine drugs Review Tiny Microbes with a Big Impact: The Role of Cyanobacteria and Their Metabolites in Shaping Our Future Sophie Mazard 1, Anahit Penesyan 1, Martin Ostrowski 1, Ian T. Paulsen 1,* and Suhelen Egan 2 1 Department of Chemistry and Biomolecular Sciences, Macquarie University, Sydney NSW 2109, Australia; [email protected] (S.M.); [email protected] (A.P.); [email protected] (M.O.) 2 Centre for Marine Bio-Innovation and School of Biological Earth and Environmental Sciences, University of New South Wales, Sydney NSW 2052, Australia; [email protected] * Correspondence: [email protected]; Tel.: +61-2-9850-8152 Academic Editor: Paul Long Received: 3 March 2016; Accepted: 4 May 2016; Published: 17 May 2016 Abstract: Cyanobacteria are among the first microorganisms to have inhabited the Earth. Throughout the last few billion years, they have played a major role in shaping the Earth as the planet we live in, and they continue to play a significant role in our everyday lives. Besides being an essential source of atmospheric oxygen, marine cyanobacteria are prolific secondary metabolite producers, often despite the exceptionally small genomes. Secondary metabolites produced by these organisms are diverse and complex; these include compounds, such as pigments and fluorescent dyes, as well as biologically-active compounds with a particular interest for the pharmaceutical industry. Cyanobacteria are currently regarded as an important source of nutrients and biofuels and form an integral part of novel innovative energy-efficient designs. Being autotrophic organisms, cyanobacteria are well suited for large-scale biotechnological applications due to the low requirements for organic nutrients. Recent advances in molecular biology techniques have considerably enhanced the potential for industries to optimize the production of cyanobacteria secondary metabolites with desired functions. This manuscript reviews the environmental role of marine cyanobacteria with a particular focus on their secondary metabolites and discusses current and future developments in both the production of desired cyanobacterial metabolites and their potential uses in future innovative projects. Keywords: natural products; microalgae; biotechnology 1. Introduction Cyanobacteria are photosynthetic prokaryotes. Despite the fact they are often referred to as blue-green algae, they have no direct relation to higher algae. They are believed to be one of the oldest organisms on Earth with fossil records dating back 3.5 billion years [1,2]. Cyanobacteria are responsible for the Earth’s transition from a carbon dioxide-rich atmosphere to the present relatively oxygen-rich atmosphere as a consequence of oxygenic photosynthesis [3]. Throughout their long evolutionary history, cyanobacteria have diversified into a variety of species with various morphologies and niche habitats. Cyanobacteria present a diverse range of morph types, including unicellular, surface-attached, filamentous colony- and mat-forming species. Several species form important symbiotic associations with other micro- and macro-eukaryotes [4,5]. In keeping with the broad taxonomic diversity across the phylum, cyanobacteria inhabit a diverse range of terrestrial and aquatic habitats, ranging from deserts to freshwater and marine systems across a range of eutrophic and oligotrophic conditions. They can also be found in extreme environments, such as Antarctic dry valleys, Arctic and thermophilic Mar. Drugs 2016, 14, 97; doi:10.3390/md14050097 www.mdpi.com/journal/marinedrugs Mar. Drugs 2016, 14, 97 2 of 18 They can also be found in extreme environments, such as Antarctic dry valleys, Arctic and thermophilicMar. Drugs 2016 lakes, 14, 97 [6,7], as well as in unlikely habitats for phototrophs, such as in the subsurface2 of of 19 calcareous rocks (Gloeobacter violaceus) [8] and Lava Caves [9]. lakesThroughout [6,7], as well their as in evolutionary unlikely habitats history, for cyanobacteria phototrophs, such have as developed in the subsurface unique ofinteractions calcareous with rocks other(Gloeobacter (micro‐ violaceusand macro)[8]‐) and organisms. Lava Caves Many [9 ].of these interactions are based on a multitude of unique and complexThroughout genetic their pathways evolutionary leading history, to the cyanobacteria production of have secondary developed metabolites unique interactions[4,5]. Secondary with metabolitesother (micro- from and cyanobacteria macro-) organisms. have been Many studied of these traditionally interactions for are their based involvement on a multitude in disease, of unique e.g., microcystinsand complex and genetic cylindrospermopsin, pathways leading which to the trigger production gastrointestinal of secondary illness, metabolites liver disease [4,5 ].and Secondary kidney damage,metabolites or for from their cyanobacteria medicinal haveproperties, been studied such as traditionally anticancer, for antimicrobial their involvement and UV in disease,‐protective e.g., activities.microcystins The andlast cylindrospermopsin,decade has seen an increased which trigger interest gastrointestinal in cyanobacterial illness, research, liver disease resulting and kidney in an expansiondamage, or of for the their uses medicinal of cyanobacterial properties, such metabolites as anticancer, beyond antimicrobial the realms and of UV-protective public health activities. and pharmaceuticalThe last decade hasindustries seen an increasedto include interest pigments, in cyanobacterial food and research, fuel resultingproduction in an expansionand other of biotechnologicalthe uses of cyanobacterial applications metabolites [10,11]. beyond the realms of public health and pharmaceutical industries to includeSeveral pigments, recent publications food and fuel have production extensively and reviewed other biotechnological the diversity and applications genetics of [10 secondary,11]. metaboliteSeveral production recent publications in (marine) have cyanobacteria extensively reviewed [12–15]. theTherefore, diversity here, and geneticswe summarize of secondary this informationmetabolite productionand present in (marine)insights cyanobacteriainto the current [12 –15transition]. Therefore, of research here, we from summarize traditional this chemistryinformation‐based and presentscreens insightsto molecular into the engineering current transition and synthetic of research biology. from traditional These advances chemistry-based will not onlyscreens contribute to molecular to basic engineering knowledge, and but synthetic will also biology. further Thesedrive the advances use of willcyanobacterial not only contribute secondary to metabolitesbasic knowledge, in novel but applications. will also further drive the use of cyanobacterial secondary metabolites in novel applications. 2. Environmental Impact of Marine Cyanobacterial Secondary Metabolites 2. EnvironmentalSome of the earliest Impact research of Marine on cyanobacterial Cyanobacterial secondary Secondary metabolites Metabolites derived from the study of toxinsSome produced of the by earliest harmful research algal blooms on cyanobacterial (HAB) and was secondary mainly metabolitesfocused on freshwater derived from species the [16–18]. study of Toxintoxins production produced by by harmful HAB can algal have blooms dramatic (HAB) health and and was economic mainly focused impacts on in freshwater lakes, rivers, species estuarine [16–18 ]. andToxin coastal production shores, by resulting HAB can in have the dramatic death of health cattle and and economic domestic impacts animals, in lakes, as well rivers, as shellfish estuarine poisoning,and coastal leading shores, to resulting substantial in the financial death of loss cattle to industries and domestic (Figure animals, 1) [19]. as well as shellfish poisoning, leading to substantial financial loss to industries (Figure1)[19]. Figure 1. Environmental impact of photosynthetic microorganisms in aquatic systems. Different classes Figureof photosynthetic 1. Environmental microorganisms impact of arephotosynthetic found in aquatic microorganisms and marine environmentsin aquatic systems. where theyDifferent form classesthe base of ofphotosynthetic healthy food microorganisms webs and participate are found in symbioses in aquatic with and other marine organisms. environments However, where shifting they formenvironmental the base of conditions healthy food can webs result and in participate community in dysbiosis, symbioses where with theother growth organisms. of opportunistic However, shiftingspecies canenvironmental lead to harmful conditions blooms andcan toxin result production in community with negative dysbiosis, consequences where the to human growth health, of opportunisticlivestock and species fish stocks. can lead Positive to harmful interactions blooms areand indicated toxin production by arrows; with negative negative interactions consequences are toindicated human health, by closed livestock circles onand the fish ecological stocks. Positive model. interactions are indicated by arrows; negative interactions are indicated by closed circles on the ecological model. Mar. Drugs 2016, 14, 97 3 of 19 The structure, cellular target and bioactivity of HAB toxins are broad and include soluble compounds of several types, such as neurotoxins, hepatoxins, cytotoxins, dermatoxins, in addition to endotoxins, e.g., lipopolysaccharides (LPS). The best-studied examples of cyanobacterial toxins are the neurotoxins; anatoxin-a/saxitoxin (Anabaena flos aquae)[20,21] and the potent hepatotoxin
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