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Does the Chemical Diversity of the Order Haplosclerida (Phylum Porifera: Class Demospongia) Fit with Current Taxonomic Classification?

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Does the Chemical Diversity of the Order Haplosclerida (Phylum Porifera: Class Demospongia) Fit with Current Taxonomic Classification? Reviews 843 Does the Chemical Diversity of the Order Haplosclerida (Phylum Porifera: Class Demospongia) Fit with Current Taxonomic Classification? Authors Marie-Aude Tribalat 1, Maria V. Marra2, Grace P. McCormack 2, Olivier P. Thomas1, 3 Affiliations 1 Géoazur UMR Université Nice Sophia Antipolis-CNRS‑IRD‑OCA, Valbonne, France 2 National University of Ireland Galway, Zoology, School of Natural Sciences, University Road, Galway, Ireland 3 National University of Ireland Galway, Marine Biodiscovery, School of Chemistry, University Road, Galway, Ireland Key words Abstract help in the revision of this large group of marine l" sponges ! invertebrates. We focus only on 3-alkylpyridine l" Haplosclerida Sponges and their associated microbiota are well derivatives and polyacetylenic compounds, as l" alkaloids known to produce a large diversity of natural these two groups of natural products are charac- l" polyacetylenic products, also called specialized metabolites. In teristic of haplosclerid species and are highly di- l" chemotaxonomy addition to their potential use in the pharmaceu- verse. A close collaboration between chemists tical industry, these rather species-specific com- and biologists is required in order to fully apply pounds may help in the classification of some par- chemotaxonomical approaches, and whenever ticular sponge groups. We review herein com- possible biological data should include morpho- pounds isolated from haplosclerid sponges (Class logical and molecular data and some insight into Demospongia, Order Haplosclerida) in order to their microbial abundance. Introduction marine natural products, including alkaloids, ! polyacetylenes, or terpene derivatives. This group Sponges (Phylum Porifera) are sessile inverte- is also one of the most diverse of the sponge received Nov. 29, 2015 brates distributed in most aquatic ecosystems. In groups in terms of numbers of species and habi- revised March 8, 2016 accepted March 22, 2016 marine areas like the Caribbean Sea, they may tats, and its members also have few distinguish- represent the largest substrate cover and/or the ing morphologial characteristics. The current Bibliography largest organic biomass of living organisms, thus classification of the order as outlined in Systema DOI http://dx.doi.org/ contributing significantly to several nutrient Porifera, based primarily on morphology, is com- 10.1055/s-0042-105879 Published online May 2, 2016 cycles due to their outstanding filtering capabil- prised of three suborders [two marine (Haplo- Planta Med 2016; 82: 843–856 ities [1,2]. In addition, during their long evolu- sclerina and Petrosina) and one freshwater (Spon- © Georg Thieme Verlag KG tionary history, most, if not all, of the diverse spe- gillina)]. The marine suborders together comprise Stuttgart · New York · cies of this group (> 8000 described species to six families; Callyspongiidae, Chalinidae, Niphati- ISSN 0032‑0943 date) together with their associated microbiota dae, Petrosiidae, Phloeodictyidae, and Calcifibro- Correspondence have developed unique metabolic pathways lead- spongiidae [5]. Analysis of sterol chemistry had This document was downloaded for personal use only. Unauthorized distribution is strictly prohibited. Prof. Grace P. McCormack ing to a huge diversity of natural products, also indicated possible difficulties with their classifi- Ryan Institute School of Natural Sciences called specialized metabolites [3]. Taxonomic cation [6], suggesting patterns of relatedness that National University of Ireland classification in this particular group of marine did not agree with morphological data, while in University Road invertebrates is still highly challenging due to a contrast, a review of 3-alkylpiperidine alkaloids Galway Ireland paucity of morphological characters and a dis- appeared to agree with the current classification Phone: + 35391492321 crepancy between molecular and morpological [7]. Subsequent molecular phylogenetic studies Fax: + 353 91494535 data in many cases. For this reason, biochemical reveal an evolutionary history that is not com- [email protected] Correspondence information has been recently used as a comple- pletely compatible with Systema Porifera, indicat- Prof. Olivier P. Thomas mentary tool (particularly within the framework ing that the freshwater sponges belong elsewhere School of Chemistry of targeted or untargeted metabolomic ap- in the Demospongiae, and that while the marine National University of Ireland University Road proaches), leading to the recent concept of inte- Haplosclerida do form a clade, the suborders and Galway grative systematics [4]. the families (where there is enough data) are Ireland Within the Class Demospongiae, sponges belong- polyphyletic [8]. For this reason, a reassessment Phone: + 35391493563 Fax: + 353 91495576 ing to the Order Haplosclerida are considered of the Order Haplosclerida is underway by multi- [email protected] among the most prolific sources of bioactive ple research groups, as an assessment of chemical Tribalat M-A et al. Does the Chemical… Planta Med 2016; 82: 843–856 844 Reviews diversity may help in the development of a robust integrative Family Niphatidae classification of the group and, in return, current systematic Within the family Niphatidae, an outstanding diversity of alka- studies in this group may also direct the search for related com- loids has been isolated from members of the genus Amphimedon. pounds of interest. Monomers of 3-alkylpyridines named hachijodines E–Gaswell This review will focus on two major classes of specialized metab- as glycosylated monomers named amphimedosides A–E were olites found in the Order Haplosclerida (3-alkylpyridine deriva- isolated from Amphimedon sp. collected off Hachijo-Jima Island tives and polyacetylene derivatives) and will discuss them in (Japan; l" Fig. 1) [10,11]. Additional mono- and dimers, pyrino- view of the currently accepted classification for five of the six demins B–I, were reported from Amphimedon sp. found in the families described in Systema Porifera [5], with no compound same area (Nakijin, Okinawa) along with a high number of being reported so far from sponges of the sixth family Calcifibro- dimers bearing a hydroxylamine moiety, starting with the bis-3- spongiidae [9]. Sterols and fatty acids have been reported for alkylpyridine derivative pyrinodemin A and nakinadines A–F some members of this group in 1994 [6], and the large chemical (with a β-aminoacid) [12–16]. All of the compounds mentioned diversity produced by this prolific sponge group was last collated were found to exhibit cytotoxicity. Niphates sp. yielded some in 1996 for 3-alkylpiperidine derivatives [7]. This review is not mono-3-alkylpyridine derivatives named niphatynes A–B, again aimed to be exhaustive but discusses representatives of 3-alkyl- from the Northwestern Pacific (Fiji; l" Fig. 2) [17], and Kobaya- pyridine derivatives and polyacetylene derivatives. Given that shiʼs group more recently described some very close analogues they are both widely distributed amongst haplosclerid species, named niphatesines A–H from a Japanese sponge of the same ge- are largely restricted to this group, and are rather unique in the nus (l" Fig. 2) [18,19]. Pyrinadines A–G have been isolated from field of natural products, we consider that focusing our review Cribrochalina sp., also from the Japanese coast (l" Fig. 2) [20,21]. on these two chemical families provides ample information to It is not known if the two Amphimedons or Niphates sp. men- help identify discrepancies in the classification, areas for focus tioned here are the same species or two separate species in each in the construction of a revised integrative classification and case given that the specimens were collected in the same geo- valuable avenues for future research focus. graphical area. Comparison of the specimen vouchers from the Major issues with publishing descriptions of compounds from various studies will have to be performed to confirm if this is species that have not been fully identified will become apparent. the case and preferably also comparison of DNA sequences. This issue is relevant not only for the group of marine sponges in- It would appear that simple mono- and bis-3-alkylpyridine de- cluded here, but for any organism of interest for bioprospecting. rivatives are restricted to species belonging to the genera Amphi- Accompanying morphological identification with a DNA se- medon, Cribrochalina,andNiphates, all belonging to the family quence is a highly recommended way forward (in addition to Niphatidae (l" Table 1). While molecular data confirms that cer- deposition of a specimen voucher in a respected institute/muse- tain Niphates and Amphimedon species are related to each other, um). We intend this review to encourage better connections be- the position of Cribrochalina and Pachychalina in relation to other tween chemists and biologists in an effort to identify novel com- members of the Niphatidae family remains unresolved [22]. As pounds of interest while also striving to understand the origins more focus is placed on resolving haplosclerid taxonomy, and and evolution of the same. A solid taxonomic description and compounds are isolated from more fully described species, it will classification will help in the rational collection of closely related be interesting to confirm if this pattern remains. species that will produce a large diversity of analogues of a tar- Also, within the family Niphatidae, a dimeric cyclostellettamine geted natural
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