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Culturable Microorganisms Associated with Sea Cucumbers and Microbial Natural Products

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Culturable Microorganisms Associated with Sea Cucumbers and Microbial Natural Products marine drugs Review Culturable Microorganisms Associated with Sea Cucumbers and Microbial Natural Products Lei Chen * , Xiao-Yu Wang, Run-Ze Liu and Guang-Yu Wang * Department of Bioengineering, School of Marine Science and Technology, Harbin Institute of Technology at Weihai, Weihai 264209, China; [email protected] (X.-Y.W.); [email protected] (R.-Z.L.) * Correspondence: [email protected] or [email protected] (L.C.); [email protected] or [email protected] (G.-Y.W.); Tel.: +86-631-5687076 (L.C.); +86-631-5682925 (G.-Y.W.) Abstract: Sea cucumbers are a class of marine invertebrates and a source of food and drug. Numerous microorganisms are associated with sea cucumbers. Seventy-eight genera of bacteria belonging to 47 families in four phyla, and 29 genera of fungi belonging to 24 families in the phylum Ascomycota have been cultured from sea cucumbers. Sea-cucumber-associated microorganisms produce diverse secondary metabolites with various biological activities, including cytotoxic, antimicrobial, enzyme- inhibiting, and antiangiogenic activities. In this review, we present the current list of the 145 natural products from microorganisms associated with sea cucumbers, which include primarily polyketides, as well as alkaloids and terpenoids. These results indicate the potential of the microorganisms associated with sea cucumbers as sources of bioactive natural products. Keywords: sea cucumber; bioactivity; diversity; microorganism; polyketides; alkaloids Citation: Chen, L.; Wang, X.-Y.; Liu, 1. Introduction R.-Z.; Wang, G.-Y. Culturable Sea cucumbers are marine invertebrates that belong to the class Holothuroidea of the Microorganisms Associated with Sea phylum Echinodermata. Globally, there are about 1500 species of sea cucumbers [1], which Cucumbers and Microbial Natural are divided into three subclasses: Aspidochirotacea, Apodacea, and Dendrochirotacea, and Products. Mar. Drugs 2021, 19, 461. can be further divided into six orders: Aspidochirotida, Elasipodida, Apodida, Molpadida, https://doi.org/10.3390/md19080461 Dendrochirotida, and Dactylochirotida [2]. Sea cucumbers are found in benthic areas and the deep sea worldwide [3]. They Academic Editor: Khaled A. Shaaban play an important role in marine ecosystems and occupy a similar niche to earthworms in terrestrial ecosystems [4]. Sea cucumbers obtain food by ingesting marine sediments or Received: 20 July 2021 filtering seawater [5] and provide a unique, fertile habitat for a variety of microorganisms, Accepted: 13 August 2021 including bacteria and fungi [6]. However, since most microorganisms are unculturable Published: 16 August 2021 under conventional laboratory conditions [7], this review primarily focuses on culturable sea-cucumber-associated microorganisms. Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in Sea cucumbers have been used in medicine in Asia for a long time [8]. For example, published maps and institutional affil- an ointment derived from the sea cucumber Stichopus sp. 1 is used to treat back and iations. joint pain in Malaysia [9]. Compounds isolated from sea cucumbers have a variety of biological and pharmacological activities, such as anticancer, antiangiogenic, anticoagu- lant/antithrombotic, antioxidant, antiinflammatory, antimicrobial, antihypertension, and radioprotective properties [10,11]. A phase II clinical trial of a sea cucumber extract, called TBL-12, has been conducted in patients with untreated asymptomatic myeloma [12]. Many Copyright: © 2021 by the authors. studies have shown that the microorganisms associated with marine animals, such as Licensee MDPI, Basel, Switzerland. sponges and ascidians, are the true producers of marine natural products [13–16]. There- This article is an open access article distributed under the terms and fore, investigating sea-cucumber-associated microorganisms is essential for discovering conditions of the Creative Commons new compounds with potential as novel active drugs. For the past 20 years, there has Attribution (CC BY) license (https:// been an increasing effort made by researchers on diversity and bioactive compounds of creativecommons.org/licenses/by/ microorganisms associated with sea cucumber. However, previously, no comprehensive 4.0/). review article as such has ever been published about this field. Mar. Drugs 2021, 19, 461. https://doi.org/10.3390/md19080461 https://www.mdpi.com/journal/marinedrugs Mar. Drugs 2021, 19, x 2 of 22 Mar. Drugs 2021, 19, 461 an increasing effort made by researchers on diversity and bioactive compounds of micro-2 of 21 organisms associated with sea cucumber. However, previously, no comprehensive review article as such has ever been published about this field. This review discusses the biodiversity of the culturable microorganisms associated This review discusses the biodiversity of the culturable microorganisms associated with sea cucumbers and the chemical structure and bioactive properties of the secondary with sea cucumbers and the chemical structure and bioactive properties of the secondary metabolites produced by these microorganisms. metabolites produced by these microorganisms. 2.2. Microorganisms Microorganisms Associated Associated with with Sea Sea Cucumbers Cucumbers 2.1.2.1. Geographical Geographical Distribution Distribution of of Microorganisms Microorganisms Associated Associated with with Sea Cucumbers AlthoughAlthough sea sea cucumbers cucumbers are are distributed distributed in in oceans oceans worldwide worldwide [3] [3],, most studies on thethe biological biological and and chemical diversity of sea-cucumber-associatedsea-cucumber-associated microorganisms have focusedfocused on on species species in in the the northern northern temperate temperate areas areas and andtropical tropical areas areas of the of eastern the eastern hem- ispherehemisphere [17–2 [617].– More26]. More than than80% of 80% the of sampling the sampling sites are sites located are located on the on west the coast west of coast the Pacificof the PacificOcean. Ocean.However, However, a small anumber small numberof sampling of sampling sites are sitesalso located are also in located the Atlantic, in the Indian,Atlantic, and Indian, Antarctic and Oceans Antarctic [17 Oceans–26] (Figure [17–26 1 ]and (Figure Table1 Sand1). Sea Table cucumber S1). Sea samples cucumber are typicallysamples arecollected typically from collected the coast from at a the depth coast of atless adepth than 20 of m less [17 than–21] 20. m [17–21]. FigureFigure 1. 1. GeographicalGeographical distribution of sea cucumbercucumber samplessamples usedused forfor studies studies of of culturable culturable microor- micro- organisms.ganisms. The The red red circles circles represent represent sampling sampling sites: sites: (A) (A) Funka Funka Bay Bay and and Ainuma Ainuma fishing fishing port, port, Hokkaido, Hok- kaido,Japan; Japan; (B) Sea (B) of Japan,Sea of Russia;Japan, Russia; (C) Yellow (C) Sea,Yellow China; Sea, (D) China; Geomun-do, (D) Geomun Yeosu,-do, Korea; Yeosu, (E) Korea; Kushima, (E) Kushima,Omura; Koecho; Omura; Nagasaki; Koecho; Nagasaki; Japan; (F) Japan; Coast (F) of AkaCoast Island, of Aka Okinawa Island, Okinawa prefecture, prefecture, Japan; (G) Japan; Ningde, (G) Ningde, Fujian, China; (H) South China Sea, China; (I) Dayang Bunting Island, Yan, Kedah Darul Fujian, China; (H) South China Sea, China; (I) Dayang Bunting Island, Yan, Kedah Darul Aman, Aman, Malaysia; (J) Tioman Island, Pahang Darul Makmur; Peninsular Malaysia; Pangkor Island, Malaysia; (J) Tioman Island, Pahang Darul Makmur; Peninsular Malaysia; Pangkor Island, Perak; Perak; Malaysia; (K) Sari Ringgung, Lampung, Indonesia; (L) Larak Island, Persian Gulf, Iran; (M) Tabarka,Malaysia; Tunisia; (K) Sari and Ringgung, (N) the Lampung,Antarctic. Indonesia; (L) Larak Island, Persian Gulf, Iran; (M) Tabarka, Tunisia; and (N) the Antarctic. 2.2.2.2. Culturable Culturable Microorganisms Microorganisms Associated Associated with with Sea Sea Cucumbers Cucumbers TheThe sea sea cucumbers cucumbers used used for for the the isolation isolation of culturable of culturable microorganisms microorganisms belong belong to five to generafive genera (Holothuria (Holothuria, Cucumaria, Cucumaria, Stichopus, Stichopus, Apostichopus, Apostichopus, and, andEupentactaEupentacta) in )four in four families fami- (Holothuriidae,lies (Holothuriidae, Stichopodidae, Stichopodidae, Cucumariidae, Cucumariidae, and Scl anderodactylidae) Sclerodactylidae) (Table (Table 1). The1). dom- The inantdominant species species is Apostichopus is Apostichopus japonicus japonicus, which, which accounts accounts for about for about 41% 41%of the of total the total sea cu- sea ccucumberumber population. population. In Insecond second place place,, HolothuriaHolothuria leucospilota leucospilota aaccountsccounts for for about about 27% 27% of of the the totaltotal sea sea cuc cucumberumber population population (Table (Table S S1).1). InIn studies studies on on microorganisms microorganisms associated associated with with sea sea cucumbers, cucumbers, samples samples are are primarily primarily obtainedobtained from from the the following following body body parts: parts: the the body body wall wall [22,23] [22,23],, body body surface surface [18,21,24 [18,21,24––29]29],, innerinner body body tissue tissue [30] [30],, coelomic coelomic fluid fluid [24,31] [24,31],, stomach stomach [30] [30],, intestines intestines [4,6,17,19,2 [4,6,17,19,255,32,32––35]35],, brownbrown gastrointestinal gastrointestinal tissue [30] [30],,
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