Analysis of antimicrobial potential and functional perspectives of marine macroalgal epiphytic microbiomes from Visakhapatnam coast of Bay of Bengal, India

The macroalgae (basibiont) and associated epiphytic microbiome (epibiont) evolved as a functional unit known as ‘macroalgal holobiont’. In this non-parasitic association, the epiphytic microbial biofilm acts as a protective layer on macroalgae. A suspected but relatively unknown capability of the macroalgal epiphytic microbiome is that it secretes a vast array of secondary metabolites that ultimately help in host defence. The present study evaluated the antimicrobial potential of marine macroalgal epiphytic microbiomes using culture-dependent and -independent approaches. In the culture-dependent approach, 271 bacterial strains were isolated from 61 different macroalgal host samples representing 16 genera of macroalgae, and their antibacterial activity was screened using a microbiological assay. Thirty-one bacterial isolates showed antibacterial activity against common bacterial pathogens; most (~75%) were identified as Bacillus species. In the culture-independent approach, we sequenced the metagenome of seven selected macroalgal epiphytic microbiomes. A total of 236 putative biosynthetic gene clusters (BGCs) were predicted from seven metagenomic libraries, which represent 12 different classes of BGCs. Non-ribosomal peptide synthetase (NRPS) was the most abundant (20%), followed by terpene (18%). Other notable clusters were ribosomally synthesized and post-translationally modified peptides (RiPP-like; 13%), homoserine lactone (Hserlactone; 13%), Ectoine (9%), type 1 polyketide synthase (T1PKS; 8%), and RiPP Recognition Element (RRE)-containing (8%) types. Overall, the integrative screening effort suggests that the macroalgal epiphytic microbiome could be the potential reservoir for future novel antimicrobial compound discovery. In addition, detecting several acyl homoserine-lactone (AHL) encoding BGCs in the metagenome dataset indicates their essential role in macroalgal epiphytic microbial colonization via quorum sensing (QS). Similar types of BGCs encoded by taxonomically distinct microbial species were observed from different hosts, suggesting that they could be functionally equivalent within the microbiomes. ~11% of total macroalgal epiphytic bacterial isolates showed antibacterial activity.Twelve classes of biosynthetic gene clusters (BGCs) reported from microbiomes.Non-ribosomal peptide synthetase (NRPS) was most abundant BGC in microbiomes. ~11% of total macroalgal epiphytic bacterial isolates showed antibacterial activity. Twelve classes of biosynthetic gene clusters (BGCs) reported from microbiomes. Non-ribosomal peptide synthetase (NRPS) was most abundant BGC in microbiomes.