Bacterial symbioses of the medicinal leech Hirudo verbana

Figures & data

Figure 1. Major alimentary structures and microbial interactions of Hirudo verbana. Drawing demonstrating the anatomy of Hirudo verbana showing the major structures of the alimentary system including the crop, lateral crop ceca, nephridia and bladders, intestinum, and anus. Inset images illustrate microbial interactions within the bladder (A), along the crop epithelium (B) and through the crop at large (C) and are as follows: A) FISH image showing the distribution of bacteria within the bladder lumen (colors correspond to probes targeted as follows: green = β-Proteobacteria, red = Bacteroidetes, blue = Bacteria); (B) FISH image of the Rikenella-like bacterium (red) along the crop epithelium, epithelial cell nuclei counter-stained with DAPI; (C1) composite image of Aeromonas (red) associated with the cell surface of a leech hemocyte, nucleus counter-stained with DAPI; (C2) FISH image of mixed microcolonies showing both Aeromonas (green) and the Rikenella-like bacterium (red), erythrocytes from a blood meal auto-fluoresce green and have darkened interiors; (C3) fluorescent image of lectin staining using succinylated wheat germ agglutinin (WGA-S, red) and DAPI counter-staining of bacterial colonies. For images A and B, the following indicators are used: E indicates the tissue epithelium of the bladder (A) or crop (B) and L indicates the lumen.

Table 1. List of Aeromonas veronii mutants

Functional Group	Strain ID(s)	Identified defect/mutation	Colonization deficiency*	Reference for strain
Parent/Wild-type Strains	HM21R, HM21RS	-	-	24
Complement Resistance	30+ isolates	Multiple genetic loci	+, ++, +++	59
Oxidative Stress	JG186	katA	-	72
Surface Modification	JG356	Glycosyltransferase	+++	59
	JG736, JG730	lpp	+++	59, Bomar and Graf unpublished
	JG738	Methyltransferase type 11	++	59
Regulatory	JG574	Ribosomal operon	+	59
	JG697	GTP-binding protein	++	59
	JG741	Exoribonuclease II	+	59
Nutrition	JG537	pstC homolog	++	59
	JG698	GufA	+	59
	JG750	Threonine/serine transporter	++	59
Host Interaction	JG752	ascU - Type III secretion system	++	70
	HE-1095	exeM - Type II secretion system	+	69
Unknown Role	JG521, JG573, JG735, JG751	Hypothetical proteins	+, ++, +++	59
	JG532	Conserved hypothetical protein	+	59
	JG533	KAP family P-loop domain protein	+	59
	JG538	Peptidase S15	+	59
	JG523, JG753	No similar BLAST result	+	59

* Colonization deficiency of leech crop compared with parent/wild-type strain represented as follows: -, no colonization deficiency; +, 2–10 fold deficiency; ++, 10–100 fold deficiency; +++, > 100 fold deficiency

Graf J. Symbiosis of Aeromonas veronii biovar sobria and Hirudo medicinalis, the medicinal leech: a novel model for digestive tract associations. Infect Immun 1999; 67:1 - 7; PMID: 9864188

 PubMed Web of Science ®Google Scholar

Silver AC, Rabinowitz NM, Küffer S, Graf J. Identification of Aeromonas veronii genes required for colonization of the medicinal leech, Hirudo verbana. J Bacteriol 2007; 189:6763 - 72; http://dx.doi.org/10.1128/JB.00685-07; PMID: 17616592

 PubMed Web of Science ®Google Scholar

Rio RVM, Anderegg M, Graf J. Characterization of a catalase gene from Aeromonas veronii, the digestive-tract symbiont of the medicinal leech. Microbiology 2007; 153:1897 - 906; http://dx.doi.org/10.1099/mic.0.2006/003020-0; PMID: 17526846

 PubMed Web of Science ®Google Scholar

Silver AC, Kikuchi Y, Fadl AA, Sha J, Chopra AK, Graf J. Interaction between innate immune cells and a bacterial type III secretion system in mutualistic and pathogenic associations. Proc Natl Acad Sci U S A 2007; 104:9481 - 6; http://dx.doi.org/10.1073/pnas.0700286104; PMID: 17517651

 PubMed Web of Science ®Google Scholar

Maltz M, Graf J. The type II secretion system is essential for erythrocyte lysis and gut colonization by the leech digestive tract symbiont Aeromonas veronii. Appl Environ Microbiol 2011; 77:597 - 603; http://dx.doi.org/10.1128/AEM.01621-10; PMID: 21097598

 PubMed Web of Science ®Google Scholar