Natural Products from Tongan Marine Organisms

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Natural Products from Tongan Marine Organisms molecules Review Natural Products from Tongan Marine Organisms Taitusi Taufa 1 , Ramesh Subramani 1,† , Peter T. Northcote 2 and Robert A. Keyzers 3,* 1 School of Agriculture, Geography, Environment, Ocean and Natural Sciences (SAGEONS), Laucala Campus, The University of the South Pacific, Suva, Fiji; [email protected] 2 Ferrier Research Institute and Centre for Biodiscovery, Victoria University of Wellington, Wellington 6140, New Zealand; [email protected] 3 School of Chemical and Physical Sciences, Centre of Biodiscovery, Victoria University of Wellington, Wellington 6140, New Zealand * Correspondence: [email protected]; Tel.: +64-4-463-5117 † Dedicated to the memory of author Ramesh Subramani, who passed away during the preparation of this manuscript. Abstract: The islands of the South Pacific Ocean have been in the limelight for natural product biodiscovery, due to their unique and pristine tropical waters and environment. The Kingdom of Tonga is an archipelago in the central Indo-Pacific Ocean, consisting of 176 islands, 36 of which are inhabited, flourishing with a rich diversity of flora and fauna. Many unique natural products with interesting bioactivities have been reported from Indo-Pacific marine sponges and other invertebrate phyla; however, there have not been any reviews published to date specifically regarding natural products from Tongan marine organisms. This review covers both known and new/novel Marine Natural Products (MNPs) and their biological activities reported from organisms collected within Tongan territorial waters up to December 2020, and includes 109 MNPs in total, the majority from Citation: Taufa, T.; Subramani, R.; the phylum Porifera. The significant biological activity of these metabolites was dominated by Northcote, P.T.; Keyzers, R.A. Natural cytotoxicity and, by reviewing these natural products, it is apparent that the bulk of the new and Products from Tongan Marine interesting biologically active compounds were from organisms collected from one particular island, Organisms. Molecules 2021, 26, 4534. emphasizing the geographic variability in the chemistry between these organisms collected at https://doi.org/10.3390/ different locations. molecules26154534 Keywords: Marine Natural Products (MNPs); tropical marine organisms; Kingdom of Tonga; Academic Editors: Enrique Barrajon, biological activity Vicente Micol and María Herranz-López Received: 17 June 2021 1. Introduction Accepted: 22 July 2021 Published: 27 July 2021 MNPs are secondary metabolites produced by both micro- and macro- marine organ- isms, produced either as a result of the organism adapting to its surrounding environment Publisher’s Note: MDPI stays neutral or as a defense mechanism against predators to assist in its survival [1]. With more than 70% with regard to jurisdictional claims in of Earth’s surface covered by oceans, which are home to phyla considered to be exclusively published maps and institutional affil- marine [2], it is logical that the marine environment represents an exceptional reservoir of iations. biodiversity and, hence, biologically active natural products, many of which exhibit unique and novel chemical features. The Kingdom of Tonga (herein referred to as Tonga) harbors an abundance of unex- plored marine biomes that could be sources of new MNPs with unique biological activities. Copyright: © 2021 by the authors. The majority of Tongan marine organisms have not been investigated for natural product Licensee MDPI, Basel, Switzerland. biodiscovery. Until recently, access to Tonga for bioprospecting has been limited, and This article is an open access article as such, most Pacific-located MNP research has been reported from neighboring island distributed under the terms and groups such as Fiji, Vanuatu, and the Solomon Islands. This review covers the structures conditions of the Creative Commons and bioactivities of Tongan marine-derived NPs up to the end of 2020. Environmental Attribution (CC BY) license (https:// influences on the production of the MNPs reviewed, and their biosyntheses, are beyond creativecommons.org/licenses/by/ the scope of this manuscript and are not included. 4.0/). Molecules 2021, 26, 4534. https://doi.org/10.3390/molecules26154534 https://www.mdpi.com/journal/molecules Molecules 2021, 26, x FOR PEER REVIEW 2 of 26 Molecules 2021, 26, 4534 2 of 26 2. The Kingdom of Tonga 2. TheTonga Kingdom is an ofarchipelago Tonga comprising 36 inhabited and 140 uninhabited islands in the CentralTonga Indo-Pacific is an archipelago Ocean, situated comprising between 36 inhabited Fiji to the and west 140 and uninhabited Samoa to islandsthe northeast. in the CentralTonga is Indo-Pacific divided into Ocean, four main situated groups; between Tongatapu, Fiji to the Vava‘u, west andHa‘apai, Samoa and to ‘Eua the northeast.(Figure 1), Tongawith several is divided other into smaller four main groups groups; completing Tongatapu, the overall Vava‘u, archipelago. Ha‘apai, and The ‘Eua largest (Figure island,1), withTongatapu, several otheron which smaller the groupscapital completingof Nuku‘alofa the is overall located, archipelago. covers 257 Thekm2 largest. Geologically, island, Tongatapu,the Tonganon islands which are the comprised capital of of Nuku‘alofa two types;is most located, have covers a limestone 257 km base2. Geologically, formed from theuplifted Tongan coral islands formations are comprised while others of two consist types; of most limestone have overlaying a limestone a base volcanic formed base. from Alt- upliftedhough Tonga coral formationsis not located while in close others proximity consist of to limestone the epicenter overlaying of marine a volcanic biodiversity, base. Althoughbounded Tongaby the isPhilippines, not located the in closeMalay proximity Peninsula, to theand epicenterNew Guinea of marine [3], Tongan biodiversity, waters boundedstill have by distinct the Philippines, and exceptional the Malay marine Peninsula, life due and to their New intrinsic Guinea [ 3geographical], Tongan waters isolation still haveand the distinct presence and exceptionalof a number marine of major life ocean due cu torrents their intrinsic in the region. geographical Tonga has isolation a total andland thearea presence of 688 km of2 a with number an Exclusive of major oceanEconomic currents Zone in (EEZ) the region. of 700,000 Tonga km has2, ~1000 a total times land more area 2 2 ofthan 688 its km landwith area, an Exclusivewhich affords Economic a huge Zone diversity (EEZ) of 700,000marine kmcommunities, ~1000 times in which more thanMNP itsstudies land area,could which be undertaken. affords a huge Given diversity the lack of of marine industry communities within Tonga, in which most MNP of the studies collec- couldtion sites be undertaken. referred to herein Given thecan lackbe cons of industryidered as within “pristine” Tonga, marine most ecosystems. of the collection sites referred to herein can be considered as “pristine” marine ecosystems. FigureFigure 1.1. Map of the the Kingdom Kingdom of of Tonga. Tonga. Image Image courtesy courtesy of ofthe the Ministry Ministry of Lands, of Lands, Survey Survey and andNat- Naturalural Resources, Resources, Tonga. Tonga. Molecules 2021, 26, 4534 3 of 26 3. Tropical Marine Organisms and Biodiversity in Tongan Territorial Waters Tropical marine ecosystems harboring a rich diversity of micro-and macro-organisms, including invertebrates, tend to produce larger quantities of structurally diverse metabolites when compared to those from temperate environments [4,5]. This latitudinal hypothesis suggests that chemical defense is mainly driven by predation pressure, and as a result, tropical organisms have evolved to have more effective defenses to deter predators and encroachment, hence having higher chemical diversity [6]. Alternatively, this correlation between source latitude and chemical defense may be attributed in part to a lack of bioprospecting investigations in temperate or polar regions. Studies have shown that organisms from the Antarctic region have comparable levels of bioactivity to those from temperate and perhaps even tropical environments [7]. In addition, Becerro et al. suggested that chemical defenses of tropical and temperate sponges might be equally effective [8]. Tonga has a unique biologically diverse marine environment, influenced by its ge- ographical isolation and the number of major ocean currents in the region. Its marine ecosystem comprises of a number of different and unique species inhabiting the pelagic and coastal areas, including thousands of fish species, marine mammals, turtles, mollusks, crustaceans, urchins, sea cucumbers, and marine algae (seaweeds). A report in 2006 in- dividually identified 202 coral, 150 mollusk, 59 echinoderm, 16 algal, and 54 polychaete worm species in Tongan territorial waters [9]. However, the overall numbers regarding Tongan marine biodiversity is still unknown. 4. A Brief History of Marine Natural Products from Tongan Waters The research group of Professor Philip Crews from the University of California at Santa Cruz (UCSC, Santa Cruz, CA, USA) conducted the first chemical investigations of Tongan marine organisms [10–13]. This was followed by several natural products studies reported by the Frederick National Laboratory for Cancer Research at Maryland, USA, however, the Coral Reef Research Foundation (CRRF, Koror, Palau) conducted the collections of the organisms [14–16]. It should be noted that both organizations were under contract to the United States of America National Cancer Institute
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