Macrobdella decora: Old World Leech Gut Microbial Community Structure Conserved in a New World Leech

Abstract

24Leeches are found in terrestrial, aquatic, and marine habitats on all continents. Sanguivorous 25 leeches have been used in medicine for millennia. Modern scientific uses include studies of 26 neurons, anticoagulants, and gut microbial symbioses. Hirudo verbana, the European medicinal 27 leech, maintains a gut community dominated by two bacterial symbionts, Aeromonas veronii and 28Mucinivorans hirudinis, which sometimes account for as much as 97% of the total crop 29 microbiota. The highly simplified gut anatomy and microbiome of H. verbana make it an 30 excellent model organism for studying gut microbial dynamics. The North American medicinal 31 leech, Macrobdella decora, is a hirudinid leech native to Canada and the northern U.S.A. In this 32 study we show that M. decora symbiont communities are very similar to those in H. verbana. 33 This similarity allowed for an extensive study in which wild caught animals were sampled to 34 determine effects of geographic separation, time of collection, and feeding on the microbiome. 35Through 16S V4 rRNA deep sequencing we show that: i) the M. decora gut and bladder 36 microbial communities are distinct, ii) the M. decora gut community is affected by feeding and 37 long periods of starvation, and iii) geographic separation does not appear to affect the overall gut 38 microbial community structure. We propose that M. decora is a replacement for H. verbana for 39 studies of wild-caught animals and offer evidence for the conservation of annelid symbionts. 40Successful culturing and comparison of dominant symbionts from M. decora and H. verbana 41 will provide the ability to assess host-symbiont co-evolution in future work. 42 43 44 45 IMPORTANCE 46 48 difficulty of assigning causative relationships in complex gut microbiomes a simplified model 49 for testing hypotheses is necessary. Previous research in Hirudo verbana has suggested this 50 animal as a highly simplified and tractable animal model of gut symbioses. Our data show that 51Macrobdella decora may work just as well as H. verbana without the drawback of being an 52 endangered organism and with the added convenience of easy access to field-caught specimens. 53The similarity of the microbial community structure of species from two different continents 54 reveals the highly-conserved nature of the microbial symbionts in sanguivorous leeches and 55 confirms the medicinal leech as a highly simplified, natural animal model in which to study gut 56 symbioses. 57 58 59 4), resulting in the name medicinal leech, Hirudo medicinalis Linnaeus, 1758. As our 64 understanding of hirundinid taxonomy improved, Hirudo medicinalis was subdivided into 65 additional species including H.verbana Carena 1820 and H.orientalis Utevsky & Trontelj, 2005 66 (5, 6). Since 2004 in the United States, only H. medicinalis and H. verbana are approved for use 67as a medical device and must be shipped from suppliers in Europe (5). Although it shares the 68 same common name, the North American medicinal leech, Macrobdella decora, was rarely used 69 ...

Horizontal gene transfer to a defensive symbiont with a reduced genome amongst a multipartite beetle microbiome

“…Interestingly, the alphaproteobacterial genus Ochrobactrum (family Brucellaceae in the NCBI taxonomy, Rhizobiaceae in GTDB) was a major putative gene donor. This genus includes several symbionts of termites (Mathew et al, 2012), army worms (Jones et al, 2019), weevils (Montagna et al, 2015) and leeches (McClure et al, 2019; Rio et al, 2009). In previous 16S amplicon investigations of Lagria beetles, Ochrobactrum were often found (Flórez et al, 2017; Flórez and Kaltenpoth, 2017) (Fig.…”

The Hirudo Medicinalis Microbiome Is a Source of New Antimicrobial Peptides

“…The genus Aminobacter belongs to the order Rhizobiales , representatives of this order are components of the microbiota from the mucus and skin of the leech [ 36 , 37 ]. Representatives of bacteria of the class Sphingobacteriia and Chitinophagia are associated with metagenomes of the skin and excretory system of leeches [ 37 , 38 ]. For example, bacteria from the genus Niabella (Class Chitinophagia ) can be found in leech cocoons, during the development of the leech, these bacteria colonize the bladder of the leech [ 39 ].…”

Horizontal Gene Transfer to a Defensive Symbiont with a Reduced Genome in a Multipartite Beetle Microbiome

“…Interestingly, the alphaproteobacterial genus Ochrobactrum (family Brucellaceae in the NCBI taxonomy and Rhizobiaceae in GTDB) was a major putative gene donor. This genus includes several symbionts of termites (79), army worms (80), weevils (81), and leeches (82,83). In previous 16S amplicon investigations of Lagria beetles, Ochrobactrum spp.…”