The chemosensory appendage proteome of Amblyomma americanum (Acari: Ixodidae) reveals putative odorant-binding and other chemoreception-related proteins

Authors: RENTHAL, ROBERT - University Of Texas At San Antonio; MAGHNANI, LEENA - University Of Texas At San Antonio; BERNAL, SANDRA - University Of Texas At San Antonio; QU, YANYAN - University Of Texas At San Antonio; GRIFFITH, WENDELL - University Of Texas At San Antonio; Lohmeyer, Kimberly - Kim; Guerrero, Felicito; BORGES, LIGIA - Federal University Of Goias; Perez De Leon, Adalberto - Beto

Submitted to: Insect Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/29/2016
Publication Date: 6/16/2016
Citation: Renthal, R., Maghnani, L., Bernal, S., Qu, Y., Griffith, W., Lohmeyer, K.H., Guerrero, F., Borges, L., Perez de Leon, A.A. 2016. The chemosensory appendage proteome of Amblyomma americanum (Acari: Ixodidae) reveals putative odorant-binding and other chemoreception-related proteins. Insect Science. 00:1-13.

Interpretive Summary: Protein analyses were conducted on two appendages of the lone star tick that sense chemicals in its surroundings. Proteins from the Haller's organ, which is a minute cavity at the terminal segment of the first pair of a tick's legs, and from the mouthparts were compared with proteins from the terminal segment of the third pair of legs. Additionally, male and female ticks were compared to each other. Proteins were identified by sequence similarities to other known proteins, compared by computer model analysis. Analysis were also done against genes expressed in the southern cattle fever tick. The terminal segment of the first pair of a tick's leg expresses a protein called lipocalin, which is not found in the distal segment of the third pair of legs, or in the mouthparts. The first leg’s terminal segment and mouthparts expressed two proteins, which are similar to insect odorant-binding proteins. Four proteins similar to the antibiotic protein microplusin were found - two exclusively in the first leg’s terminal segment, and one exclusively expressed in the mouthparts. Proteins similar to dust mite allergens were found expressed in the first leg’s terminal segment of female ticks. A protein exclusively expressed in the first leg’s terminal segment has similarities to Neto, which is known to be involved in the clustering of ligand-gated ion channels activated by the neurotransmitter glutamate. These results are the first report of insect odorant-binding protein sequences in ticks.

Technical Abstract: Proteomic analyses were done on 2 chemosensory appendages of the lone star tick, Amblyomma americanum. Proteins in the fore tarsi, which contain the olfactory Haller's organ, and in the palps, that include gustatory sensilla, were compared with proteins in the third tarsi. Also, male and female ticks were compared. Proteins were identified by sequence similarity to known proteins, and by 3-dimensional homology modeling. Proteomic data were also compared with organ-specific transcriptomes from the tick Rhipicephalus microplus. The fore tarsi express a lipocalin not found in the third tarsi or palps. The fore tarsi and palps abundantly express 2 proteins, which are similar to insect odorant-binding proteins (OBPs). Compared with insect OBPs, the tick OBP-like sequences lacked the cysteine absent in C-minus OBPs, and 1 tick OBP-like sequence had additional cysteines that were similar to C-plus OBPs. Four proteins similar to the antibiotic protein microplusin were found: 2 exclusively expressed in the fore tarsi and 1 exclusively expressed in the palps. These proteins lack the microplusin copper-binding site, but they are modeled to have a significant internal cavity, potentially a ligand-binding site. Proteins similar to the dust mite allergens Der p7 and Der f 7 were found differentially expressed in female fore tarsi. A protein exclusively expressed in the fore tarsi has similarities to Neto, which is known to be involved in clustering of ionotropic glutamate receptors. These results constitute the first report of OBP-like protein sequences in ticks and point to several research avenues on tick chemosensory reception.