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. 2020 Apr 29;21(1):331.
doi: 10.1186/s12864-020-6748-0.

Draft genome sequences of Hirudo medicinalis and salivary transcriptome of three closely related medicinal leeches

Vladislav V Babenko  1 , Oleg V Podgorny  2   3 , Valentin A Manuvera  2   4 , Artem S Kasianov  4   5 , Alexander I Manolov  2 , Ekaterina N Grafskaia  2   4 , Dmitriy A Shirokov  2 , Alexey S Kurdyumov  2 , Dmitriy V Vinogradov  6   7 , Anastasia S Nikitina  2   4 , Sergey I Kovalchuk  2   8 , Nickolay A Anikanov  2   8 , Ivan O Butenko  2 , Olga V Pobeguts  2 , Daria S Matyushkina  2 , Daria V Rakitina  2 , Elena S Kostryukova  2 , Victor G Zgoda  9 , Isolda P Baskova  10 , Vladimir M Trukhan  11 , Mikhail S Gelfand  6   7   12   13 , Vadim M Govorun  2   4 , Helgi B Schiöth  11   14 , Vassili N Lazarev  2   4
Affiliations

Draft genome sequences of Hirudo medicinalis and salivary transcriptome of three closely related medicinal leeches

Vladislav V Babenko et al. BMC Genomics. .

Erratum in

Abstract

Background: Salivary cell secretion (SCS) plays a critical role in blood feeding by medicinal leeches, making them of use for certain medical purposes even today.

Results: We annotated the Hirudo medicinalis genome and performed RNA-seq on salivary cells isolated from three closely related leech species, H. medicinalis, Hirudo orientalis, and Hirudo verbana. Differential expression analysis verified by proteomics identified salivary cell-specific gene expression, many of which encode previously unknown salivary components. However, the genes encoding known anticoagulants have been found to be expressed not only in salivary cells. The function-related analysis of the unique salivary cell genes enabled an update of the concept of interactions between salivary proteins and components of haemostasis.

Conclusions: Here we report a genome draft of Hirudo medicinalis and describe identification of novel salivary proteins and new homologs of genes encoding known anticoagulants in transcriptomes of three medicinal leech species. Our data provide new insights in genetics of blood-feeding lifestyle in leeches.

Keywords: Anticoagulants; Genome; Haematophagy; Leech H. medicinalis; Systems biology.

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Conflict of interest statement

The authors declare no competing financial interests.

Figures

Fig. 1
Fig. 1
The H. medicinalis genome binning. a. 2D-plot showing the contig distribution in coordinates of GC content and coverage by a combination of reads obtained by Ion Proton and Illumina. Contigs are indicated by dots, and the taxonomic affiliation of contigs at the domain level is encoded by colour (green – Bacteria, blue – Eukarya, black – no assignment). The taxonomic affiliation was determined by direct BlastN (megablast) search against the National Center for Biotechnology Information (NCBI) nt database. The 3D plot showing the contig distribution in coordinates of GC content, read coverage (Proton and Illumina), and host cDNA read coverage is presented in Supplementary Data 2. bH. medicinalis genome contains clusters of blood meal-related genes. The graph shows the exon-intron structure of genes and arrangement of gene clusters in scaffolds on a general scale. The exon arrows indicate the direction of transcription (gray - unknown gene)
Fig. 2
Fig. 2
Differential expression analysis of salivary cells. (a) Isolation of salivary cells and muscles by laser microdissection. MA-plots of differentially expressed genes in the salivary cells and muscles of H. medicinalis for the de novo assembled transcriptome (b) and the genome model (c). MA-plots representing the log Fold Change (logFC) against the log-average log CPM per each transcript cluster across each pair of compared samples (muscle and salivary cells). Differentially expressed clusters supported by FDR < 0.05 are plotted in red
Fig. 3
Fig. 3
Summary of the identified SCS components. The Venn diagrams in the upper panel show the numbers of ortholog clusters identified by differential expression (DE) and proteomic (Prot) analyses across three medicinal leech species. The histogram in the middle panel features the numbers of orthologous clusters identified by the differential expression analysis, proteomic analysis or a combination thereof (DE + Prot). Each bar consists of ortholog clusters identified as known blood feeding-related components (identified), other known proteins (other), and unknown proteins (NA). The pie charts in the lower panel illustrate the abundance of the individual SCS components identified by the differential expression analysis, proteomic analysis or their combination. For details, see Supplementary Tables 10, 11, and 13
Fig. 4
Fig. 4
Multiple sequences alignment of Antistasin-like transcripts with dual domain antistasin-type protease inhibitors from leeches’ Antistasin (Haementeria officinalis, P15358), Ghilantein (Haementeria ghilianii, P16242) and Eisenstasin II from earthworm (Eisenia andrei, Q5D2M8). The boxes indicates antistasins-like domane. Alignment is generated by MUSCLE algorithm, residues are colored according to ClustalX colour scheme, conserved amino acids are colorized by conservation level (threshold > 50%). Reference sequence are marked purple
Fig. 5
Fig. 5
a Alignment of CRISP domains with diverse CAP/CRISP proteins. Putative platelet inhibitors from Ancylostoma caninum (Q962V9) and Tabanus yao (C8YJ99), CAP domain containing proteins from Vampire Snail (Cumia reticulata, QBH70087.1; QBH70092.1) and reptile Cystein-rich venom proteins triflin (Protobothrops flavoviridis), natrin-2 (Naja atra) and other. Alignment is generated by MUSCLE algorithm, residues are colored according to ClustalX colour scheme, conserved amino acids are colorized by conservation level (threshold > 50%). Reference sequence are marked purple. b Alignment of new “Cys-rich” domains. The boxes indicates two cysteine patterns, amino acids are colorized by percentage Identity coloring scheme
Fig. 6
Fig. 6
a Amino acid sequences alignment of Eglin-like transcripts with Eglin (Hirudo medicinalis, P01051), hypothetical protein (Helobdella robusta, xp_009019226.1) and chymotrypsin inhibitor homolog from Potato (Solanum tuberosum, P01052). Alignment is generated by MUSCLE algorithm, residues are colored according to ClustalX colour scheme. Identical and conserved residues indicated respectively by asterisk, period and colon. b Alignment of PAN domains with leech anti-platelet protein (Haementeria officinalis, Q01747) and putative anti-platelet-like protein (Haementeria vizottoi, A0A0P4VN18). Conserved amino acids are colorized by conservation level (threshold > 75%). Reference sequence are marked purple
Fig. 7
Fig. 7
Alignment of the hirudo vWFA domains with the human vWFA1 (EAW88814.1) and vWFA1-like (Colubraria reticulata, SPP68597.1). Alignment is generated by MUSCLE algorithm, residues are colored according to ClustalX colour scheme. Identical and conserved residues indicated respectively by asterisk, period and colon. Reference sequence are marked purple
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