Chemistry, Chemotaxonomy and Biological Activity of the Latrunculid Sponges (Order Poecilosclerida, Family Latrunculiidae)

Abstract

Marine sponges are exceptionally prolific sources of natural products for the discovery and development of new drugs. Until now, sponges have contributed around 30% of all natural metabolites isolated from the marine environment. Family Latrunculiidae Topsent, 1922 (class Demospongiae Sollas, 1885, order Poecilosclerida Topsent, 1928) is a small sponge family comprising seven genera. Latrunculid sponges are recognized as the major reservoirs of diverse types of pyrroloiminoquinone-type alkaloids, with a myriad of biological activities, in particular, cytotoxicity, fuelling their exploration for anticancer drug discovery. Almost 100 pyrroloiminoquinone alkaloids and their structurally related compounds have been reported from the family Latrunculiidae. The systematics of latrunculid sponges has had a complex history, however it is now well understood. The pyrroloiminoquinone alkaloids have provided important chemotaxonomic characters for this sponge family. Latrunculid sponges have been reported to contain other types of metabolites, such as peptides (callipeltins), norditerpenes and norsesterpenes (trunculins) and macrolides (latrunculins), however, the sponges containing latrunculins and trunculins have been transferred to other sponge families. This review highlights a comprehensive literature survey spanning from the first chemical investigation of a New Zealand Latrunculia sp. in 1986 until August 2020, focusing on the chemical diversity and biological activities of secondary metabolites reported from the family Latrunculiidae. The biosynthetic (microbial) origin and the taxonomic significance of pyrroloiminoquinone related alkaloids are also discussed.

Keywords: Latrunculiidae; bioactivity; biosynthetic origin; callipeltin; chemotaxonomy; latrunculid sponge; pyrroloiminoquinone alkaloid; taxonomy.

Figure 1

Living Latrunculiidae sponges and their diagnostic spicules. Genus Strongylodesma Levi, 1969, is not represented here because they lack the diagnostic discorhabds. Species in subgenus Latrunculia (Latrunculia) have anisodiscorhabd microscleres with six visibly distinct substructures: (A) L. (L.) austini Samaai, Gibbons & Kelly, 2006, Gulf of Alaska (reproduced from reference [21], Figure 3F, with permission from copyright holder); (B) Typical anisodiscorhabd, undescribed species from the Chatham Islands, New Zealand. Species in subgenus Latrunculia (Biannulata) have anisodiscorhabd microscleres with two distinct substructures around the shaft, the median and subsidiary whorls, between an undifferentiated manubrium and basal whorl, and the undifferentiated apical whorl and apex: (C) L. (B.) kaakaariki Alvarez, Bergquist & Battershill, 2002, Three Kings Islands, New Zealand (reproduced with permission from Crispin Middleton); (D) Typical anisodiscorhabd from the same species. Species in subgenus Latrunculia (Uniannulata) have anisodiscorhabd microscleres with only a single substructure around the shaft, the median whorl, between the manubrium and basal whorl, and the apical whorl and apex: (E) L. (U.) oparinae Samaai & Krasokhin, 2002, Aleutian Islands, Alaska (reproduced with permission from Robert Stone; reproduced from reference [21], Figure 8A, with permission from copyright holder); (F) Typical anisodiscorhabd from the same species. Species in genus Cyclacanthia are Latrunculiidae with acanthose isospinodiscorhabd microscleres which have a shaft bearing identical apical and basal substructures: (G) Cyclacanthia bellae Samaai, Gibbons, Kelly & Davies-Coleman, 2003 (reproduced with permission from the Coral Reef Research Foundation, Palau, Micronesia; reproduced from reference [26], Figure 3A, with permission from copyright holder); (H) Typical isospinodiscorhabd (reproduced from reference [21], Figure 1D, with permission from copyright holder). Species in genus Tsitsikamma are Latrunculiidae with acanthose isospinodiscorhabd microscleres which have a shaft bearing identical apical and basal substructures: (I) Tsitsikamma favus Samaai & Kelly, 2002, Algoa Bay, South Africa (reproduced with permission from the Coral Reef Research Foundation, Palau, Micronesia; reproduced from reference [41], Figure 8E, with permission from copyright holder); (J) Typical isochiadiscorhabd from the same species (reproduced from reference [21], Figure 1E, with permission from copyright holder). Species in genus Bomba are Latrunculiidae with unusual anisodiscorhabds that have only three substructures: (K) Bomba endeavorensis Kelly, Reiswig & Samaai, 2016, Endeavour Ridge, British Columbia (reproduced from reference [21], Figure 11A, with permission from copyright holder); (L) Typical anisodiscorhabd from the same species. Species in genus Latrunclava are Latrunculiidae with two microsclere forms, an anisodiscorhabd and several longer anisoconicorhabds that have structurally different apical and basal whorls, unlike Sceptrella species which also have two microsclere forms, but the longer amphiclad sceptre has identical apical and basal whorls: (M) Latrunclava imago Kelly, Reiswig & Samaai, 2016, Aleutian Islands (reproduced from reference [21], Figure 13A, with permission from copyright holder); (N) Anisodiscorhabd and long anisoconicorhabd (reproduced from reference [21], Figure 1G, with permission from copyright holder); (O) Anisodiscorhabd and amphiclad sceptre from Sceptrella regalis Schmidt, 1870 (reproduced from reference [21], Figure 1F, with permission from copyright holder). All images are reproduced with permission from the original photographers or from Zootaxa.

Figure 2

Skeleton of monomeric discorhabdin-type alkaloids.

Figure 3

Discorhabdin monomers reported from latrunculid sponges. ?: Unassigned stereochemistry; *: Relative configuration; ^§: Artifact.

Figure 4

Discorhabdin oligomers reported from latrunculid sponges. *: Relative configuration.

Figure 5

Tsitsikammamines reported from latrunculid sponges. ^§: Artifact; ^&: Reported from Zyzzya sp.

Figure 6

Chemical structure of atkamine and aleutianamine.

Figure 7

Citharoxazole, batzelline, and makaluvamine reported from the genus Latrunculia. ?: Unassigned stereochemistry.

Figure 8

Callipeltins reported from the genus Latrunculia.

Figure 8

Callipeltins reported from the genus Latrunculia.

Figure 8

Callipeltins reported from the genus Latrunculia.

Scheme 1

Proposed biosynthetic pathway of discorhabdins and structurally related metabolites (adapted from references [34,40,49,82,141]).