Transcriptomic profiling of immune‐associated molecules in the coelomocytes of lugworm Arenicola marina (Linnaeus, 1758)

Abstract

Organization and functioning of immune system remain unevenly studied in different taxa of lophotrochozoan animals. We analyzed transcriptomic data on coelomocytes of the lugworm Arenicola marina (Linnaeus, 1758; Annelida, Polychaeta) to gain insights into the molecular mechanisms involved in polychaete immunity. Coelomocytes are specialized motile cells populating coelomic fluid of annelids, responsible for cellular defense reactions and providing humoral immune factors. The transcriptome was enriched with immune‐related transcripts by challenging the cells in vitro with lipopolysaccharides of Escherichia coli and Zymosan from Saccharomyces cerevisiae. Our analysis revealed a multifaceted and complex internal defense system of the lugworm. A. marina possesses orthologs of proto‐complement‐like factors: six thioester‐containing proteins, a complement‐like receptor, and a MASP‐related serine protease (MReM2). A. marina coelomocytes employ pattern‐recognition receptors to detect pathogens and regulate immune responses. Among them, there are 18 Toll‐like receptors and various putative lectin‐like proteins with evolutionary conserved and taxa‐specific domains. C‐type lectins and a novel family of Gal‐binding and CUB domains containing receptors were the most abundant in the transcriptome. The array of pore‐forming proteins in the coelomocytes was surprisingly reduced compared to that of other invertebrate species. We characterized a set of conserved proteins metabolizing reactive oxygen species and nitric oxide and expanded the arsenal of potential antimicrobial peptides. Phenoloxidase activity in immune cells of lugworm is mediated only by laccase enzyme. The described repertoire of immune‐associated molecules provides valuable candidates for further functional and comparative research on the immunity of annelids.

Novel β-Hairpin Peptide from Marine Polychaeta with a High Efficacy against Gram-Negative Pathogens

“…First, we found three peptides in Arenicola marina (NCBI accession number SRX1015734) named arenicin-4, -5, and -6. Arenicin-4, designated as ANN4, was described earlier when a transcriptomic profiling of coelomocytes of lugworm A. marina was performed [ 9 ]. Arenicin-5 has the highest homology with arenicin-4 whereas arenicin-6 is an analog of anenicin-2 with the amino acid substitution of N -terminal arginine residue for glycine.…”

Novel BRICHOS-Related Antimicrobial Peptides from the Marine Worm Heteromastus filiformis: Transcriptome Mining, Synthesis, Biological Activities, and Therapeutic Potential

“…After digestion, we did not observe two terminal parts of HfBRI-25 that pointed at the absence of C1-C2/C3-C4 pairing type. Expectedly, the major product peaks appearing in the HPLC chromatogram (peaks 2 and 3, Figure S2) corresponded to two linear fragments (4)(5)(6)(7)(8)(9)(10)(11)(12)(13)(14)(15)(16) and (19/20-25) connected by two disulfide bonds. Therefore, the β-hairpin structure with the pairing type C1-C4/C2-C3 is the most probable, which agrees well with the AlphaFold prediction data (Figure 2B and Figure S3).…”

“…Our recent results [9] and the data obtained by Bruno et al [10] have demonstrated that, in polychaetes, the BRICHOS domain might be involved in the biosynthesis of AMPs of different structural classes and not only of β-hairpin molecules. Interestingly, a detailed analysis of the A. marina transcriptome revealed two novel types of Cys-rich BRICHOSrelated peptides designated as AmIMP1 and AmIMP2 (Integral Membrane Proteins) [11]. This fact provided an additional reassurance of the hypothesis of the BRICHOS domain function as a universal and auxiliary protein module facilitating biosynthesis of various relatively hydrophobic and cysteine-containing peptides, including host defense peptides.…”