Diversity and biological activities of the bacterial community associated with the marine sponge Phorbas tenacior (Porifera, Demospongiae)

Abstract

Significance and Impact of the Study: This study presents the first report on the diversity of the cultivable bacteria associated with the marine sponge Phorbas tenacior, frequently found in the Mediterranean Sea. Evaluation of the antiplasmodial, antimicrobial and antioxidant activities of the isolates has been investigated and allowed to select bacterial strains, confirming the importance of Proteobacteria and Actinobacteria as sources of bioactive compounds.Keywords antimicrobial activity, antioxidant activity, antiplasmodial activity, associated bacteria, Phorbas tenacior, phylogenetic diversity, RAPD, sponge. AbstractThe diversity of the cultivable microbiota of the marine sponge Phorbas tenacior frequently found in the Mediterranean Sea was investigated, and its potential as a source of antimicrobial, antioxidant and antiplasmodial compounds was evaluated. The cultivable bacterial community was studied by isolation, cultivation and 16S rRNA gene sequencing. Twenty-three bacterial strains were isolated and identified in the Proteobacteria (a or c classes) and Actinobacteria phyla. Furthermore, three different bacterial morphotypes localized extracellularly within the sponge tissues were revealed by microscopic observations. Bacterial strains were assigned to seven different genera, namely Vibrio, Photobacterium, Shewanella, Pseudomonas, Ruegeria, Pseudovibrio and Citricoccus. The strains affiliated to the same genus were differentiated according to their genetic dissimilarities using random amplified polymorphic DNA (RAPD) analyses. Eleven bacterial strains were selected for evaluation of their bioactivities. Three isolates Pseudovibrio P1Ma4, Vibrio P1MaNal1 and Citricoccus P1S7 revealed antimicrobial activity; Citricoccus P1S7 and Vibrio P1MaNal1 isolates also exhibited antiplasmodial activity, while two Vibrio isolates P1Ma8 and P1Ma5 displayed antioxidant activity. These data confirmed the importance of Proteobacteria and Actinobacteria associated with marine sponges as a reservoir of bioactive compounds. IntroductionMarine sponges constitute a significant element in benthic communities in the world's oceans, in terms of both biomass and potential to participate in ecological processes. They are also recognized as a rich source of biologically active compounds (Blunt et al. 2012). Currently, five marine natural products or semisynthetic analogues isolated from sponges have been approved as therapeutics.Thirteen molecules are in clinical trials for various applications, mainly as anticancer agents, and one hundred are undergoing preclinical evaluation (Mayer et al. 2010). In the past decade, many studies have focused on the complex ecosystem sponge-microbial communities due to the association of sponges with dense and diverse microbial communities of the three domains of life (Bacteria, Archaea and Eukarya) (Taylor et al. 2007). The spongeassociated micro-organisms have revealed high densities, Letters in Applied Microbiology 58, 42--52

Exploring cultivableBacteriafrom the prokaryotic community associated with the carnivorous spongeAsbestopluma hypogea

“…All these isolates belonged to genera previously isolated from other demosponges (Taylor et al ., ; Sipkema et al ., ) including the filter‐feeding P. tenacior collected in the same geographic area (Dupont et al ., 2013b). These results suggest that marine demosponges shelter similar cultivable microbial communities.…”

“…3. Comparisons of the taxonomic affiliations at class level of Bacteria isolated from Asbestopluma hypogea cave sample (in black, CA), of sequences obtained by pyrosequencing (in gray, CA) (Dupont et al, 2013a) and from Mediterranean sponge Phorbas tenacior (in white) (Dupont et al, 2013b). Pseudomonas sp.…”

“…Complementary to former 454 pyrosequencing investigations of this carnivorous sponge prokaryote community, this study combines a culture-dependent approach, bioactivity assays, and microscopic observations to further assess and characterize the associated microorganisms from the carnivorous sponge A. hypogea. The diversity of the retrieved cultivable prokaryote community was also compared with that of the Mediterranean filter-feeding sponge Phorbas tenacior collected in the Marseille area (Dupont et al, 2013b).…”

Red Sea Suberea mollis Sponge Extract Protects against CCl4‐Induced Acute Liver Injury in Rats via an Antioxidant Mechanism

“…Recently, Lind et al [39] found that barettin isolated from the marine sponge Geodia barretti possesses antioxidant properties in ferric reducing antioxidant power (FRAP) assays and lipid peroxidation cell assays. In addition, Dupont et al [40] reported that the crude extract of the marine sponge Phorbastenacior exhibited effects against DPPH-induced oxidative stress. Suberea mollis in the order Verongida in the family Aplysinellidae afforded two new brominated arginine-derived alkaloids: subereamines A and B; a new brominated phenolic compound has exhibited strong antioxidant potential compared to vitamin E and ascorbic acid; moreover, Suberea mollis contain subereaphenol D and the known compounds dichloroverongiaquinol, aerothionin, and purealdin L [41, 42].…”

Bacterial Tropone Natural Products and Derivatives: Overview of their Biosynthesis, Bioactivities, Ecological Role and Biotechnological Potential

“…[91] They are present in all major niches, including, for example, seawater, sediments, or microbial mats. [91,92] Often, these bacteria live associated with marine invertebrates such as ascidians/tunicates, [93,94] micro [51,53] and macro algae, [68] soft and stony corals, [73,95] tube worms, [96] numerous marine sponges, [97][98][99][100][101][102][103] and many other marine eukaryotes. [104] In particular, the tendency to form strong biofilms also on biotic surfaces is a crucial prerequisite for host colonization.…”