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Molecular Characterization of Myiasis-Causing Moth Flies (Diptera: Psychodidae)/Myiasis Nedeni Guve Sineklerinin (Diptera: Psychodidae) Molekuler Karakterizasyonu.

INTRODUCTION

The Psychodidae family has a cosmopolitan distribution, with approximately 3000 described species in six subfamilies (Horaiellinae, Sycoracinae, Trichomyiinae, Bruchomyiinae, Phlebotominae, and Psychodinae) (1, 2). The subfamily Psychodinae is commonly known as the drain, moth, or filter fly because these are commonly found on the sites of buildings, such as sewers, cesspools, septic tank, sewage treatment plants, and other dark and moist places (3). The females of moth flies are not blood feeding, and they feed on flower nectar, sewage, and other moisture sources. Their larval stages are coprophagous and saprophagous, and during these stages, they feed on a gelatinous film of decaying organic matter and vertebrate faeces (4-7).

Moth flies [Psychoda and Telmastoscopus (formerly Clogmia)] of the Psychodinae subfamily are of public health and veterinary consideration (8-10). Both genera are commonly found on basement walls, in homes, and in public places such as restrooms and the bathrooms in sports centeres, hospitals, and hotels (11). When the hairs of these flies are inhaled, people cannot breathe or function comfortably, and this may even trigger respiratory problems such as allergic rhinitis and asthma in humans (7). In addition, adult moth flies can be mechanical vectors of several bacterial pathogens associated with nosocomial infections. The moth fly larvae may cause accidental myiasis (e.g, urinary, intestinal, and nasal myiasis) (4, 10, 12).

Correct species identification of the moth fly is highly important for pest control practices (13). According to external morphological characters, traditional morphological identification of the Psychodinae species is difficult (14).

At present, several DNA-based analyses have been developed for the specific identification and characterization of insect species. The mitochondrial DNA sequences have been successfully used for the identification of species in many different insect groups (15, 16). Two of the mitochondrial genes, cytochrome oxidase subunit I and II (COI and COII), are most reliable and popular molecular markers. Cytochrome c oxidase subunit I (COI) has highly conserved sequences and variable regions within vertebrates and insects (15-17). An understanding of evolutionary relationships among different subfamilies and species of the psychodid flies, especially in the moth flies, are of epidemiological importance, because the phylogenetic relationship helps to predict the mechanical transmission of bacterial pathogens such as Acinetobacter baumannii, Aeromonas hydrophila, Alcaligenes faecalis, Bacillus cereus, Escherichia coli, Klebsiella pneumoniae ssp. pneumoniae, Pseudomonas aeruginosa, P. fluorescens, and Stenotrophomonas maltophili in houses, hospitals (bathrooms, patient room toilets, and hospitals kitchens), and public toilets and bathrooms (18, 19). Therefore, the aim of this study was to determine the molecular characterization and phylogenetic status of the moth flies in Turkey.

METHODS

Collection of Samples and Genomic DNA Isolation

The fly specimens were collected from toilet, bathroom, and basement walls of houses from different locations of the Kayseri region between May 2016 and April 2017 using suitable nets. The captured flies were placed in 1.5 mL eppendorf tubes containing the 70% ethyl alcohol solution, and they were transported to the laboratory.

The whole body of each sample was crushed in a 1.5 ml microcentrifuge tube with liquid nitrogen in a pre-cooled mortar. The total DNA was extracted individually from each crushed fly using the GeneJET Genomic DNA Purification Kit (Thermo Fisher Scientific, USA) according to the manufacturer's instructions. The extracted genomic DNA samples were stored at -20[degrees]C until the PCR analyses.

PCR Amplification

Extracted DNA from each sample was used to amplify a 709 bp fragment of the mitochondrial COI gene barcoding region using the LCO-1490 forward (5'-GGTCAACAAATCATAAAGATATTGG-3') and HCO-2198 reverse (5'-TAAACTTCAGGGTGACCAAAAAATCA-3') primers (20). The concentration and purity of extracted DNA was measured by a Qubit 3.0 fuorometer (Life Technologies).

The PCR was performed in a final reaction volume of 25 [micro]L, containing 0.4 [micro]M of each primer, 0.2 mM of each dNTP (Fermentas, Vilnius, Lithuania), 50 mM KCl, 10 Mm Tris-HCl (pH 9.0), 4 mM MgCl2, 1U Taq DNA polymerase (Thermo Fisher Scientific, Hudson, NH, USA), and 50 ng of template DNA. DNase-RNase-free water was used as negative control. The reaction was performed in a C1000 Touch[TM] thermal cycler (Bio-Rad, USA), and this comprised an initial denaturation step at 94[degrees]C for 3 min, followed by 39 cycles of denaturation at 94[degrees]C for 20 sec, primer annealing at 50[degrees]C for 20 sec, and a primer extension at 72[degrees]C for 30 sec. The final extension at 72[degrees]C for 10 min was performed, and samples were held at 4[degrees]C (17). The PCR products were electrophoresed on a 1.5% agarose gel containing 10 [micro]L/mL ethidium bromide in the Tris-acetate-EDTA (TAE) buffer at 135 V for 30 min and visualized using the CLP Gel Documentation System (UVP INC Upland, CA).

Sequence Alignment and Phylogenetic and Genetic Distance Analyses

The amplifed PCR products were gel purified using the High Pure PCR product purification kit (Roche, Mannheim, Germany) following the manufacturer's instructions. In addition, purified DNA was bidirectionally sequenced (Macrogen, Korea) with the same primers used to PCR amplify a 709 bp region of the mitochondrial COI gene. The nucleotide chromatograms were aligned with the Geneious 9.1.3 software [www.geneious.com (21)]. The DNA polymorphism, the number of haplotypes, and nucleotide diversity were determined using DnaSP 5.10.01 (22). Calculations for the mean genetic diversities within and among the haplogroups were performed with the MEGA version 6 (23) by the Kimura two-parameter distance model (24, 25).

Phylogenetic analyses were performed by the Bayesian (BA) inference. The best-ft DNA-substitution model based on the Akaike information criterion algorithm was determined as the General Time Reversible (GTR) by using jModeltest v.0.1.1 (26, 27). The BA analyses were set up in the MrBayes version 3.2.6 (28) and PhyML (29), respectively, by using the plugins available with the Geneious 9.1.3 software (www.geneious.com, 21). The species of moth flies in the Genbank used for phylogenetic analysis are detailed in Table 1.

The Markov chain simulations in the BA search were run for 10 million generations, with sampling every 200 generations for the posterior probability calculations. The 25% of the parameter estimates was discarded as burn-in.

RESULTS

COI Sequences and Genetic Divergence

A total of 240 adult flies were collected from 40 houses. A total of 50 genomic DNA isolates were amplified with the PCR and sequence analyses of the partial mt-COI gene region, and all the isolates displayed a successful amplification (Figure 1).

In total, five partial sequences (658 bp without primers) of moth flies specimens from the Kayseri region were obtained. According to sequence analyses of isolates, a total of two different moth flies (ERU-Telmatos3 and ERU-Telmatos6 isolates as Telmastocopus albipunctatus and ERU-Psycho4, ERU-Psycho5, and ERU-Psycho1 as Psychodidae sp.) were identified. A total of 31 polymorphic sites were distributed among the COI sequences of the isolates, leading to the detection of three different haplotypes (isolates ERU-Telmatos3 and ERU-Telmatos6 constituted the first, ERU-Psycho4 and ERU-Psycho5 constituted the second, and ERU-Psycho1 constituted the third haplotypes). The mean haplotype diversity among the sequences was 0.800[+ or -]0.164. The base composition was strongly AT biased for all species and similar to mitochondrial genes in insects (30); the mean GC content was 0.330. All the sequences were submitted to the NCBI-gene bank nucleotide database, and the accession number assigned was KY924864-68.

Phylogenetic Analyses

The BA tree is presented in Figure 2, with posterior probability (BA) and bootstrap support (ML) values. Two major haplogroups (A and B) and one new haplotype were found in this study.

The isolates ERU-Telmatos3 and ERU-Telmatos6 were clustered with the isolates belonging to Telmatoscopus albipunctatus and Psychodidae sp., reported from India and the United States,, respectively, and they were placed under the haplogroup A1 with a high bootstrap support (100%) and posterior probability (1.00) (Figure 2). The mean genetic diversity among the isolates in the A1 haplogroup was 0.4[+ or -]0.2%. A mean genetic distance of 3.5[+ or -]0.8% was determined between the haplogroup A1 and the haplotype A2, which clustered under the major group A. The isolates ERU-Psycho4 and ERU-Psycho5 showed a 100.0% match with the isolates belonging to the Psychodidae sp. reported from Canada and constituted the B2 haplogroup with the contribution of ERU-Psycho1 isolate, which was characterized as a new haplotype (Figure 2). This phylogenetic resolution was also supported with a moderate bootstrap support (58%) and posterior probability (>0.56). The genetic difference between the ERU-Psycho1 isolate and other isolates under the B2 haplogroup was determined as 0.2[+ or -]0.2%. The B1 haplogroup included the isolates of Diptera sp. and Psychodidae sp. reported from the United States and Canada, and it showed mean genetic distances of 0.5[+ or -]0.2% to the isolates of the B2 haplogroup. The mean genetic distances between the group A and group B were designated as 5.6[+ or -]1.0%.

DISCUSSION

Psychodinae are a subfamily of the Psychodidae family and known as moth, drain, or filter flies. Approximately 2000 species within this subfamily have been described in about 100 genera distributed all over the world (31). Adult moth fly species have been reported in toilets, kitchens, bathrooms, and sewers in different geographical regions of the world (10-12, 32). Adult C. albipunctata was observed in kitchens, toilets, and bathrooms, and also in a compost heap in Belgium (5). Obona and Jezek were collecting adult C. albipunctata in and on many buildings in different districts of Slovakia (14). Similarly, in this study, adult moth flies were collected from the walls of toilets, bathrooms, and basements of buildings in Kayseri, Turkey.

Correct species identification of psychodid flies is important for pest control practices (13). The traditional morphological identification of fly species used the morphological features between species. Most authors suggested that the morphological characters of drain flies are most closely related to other insect species (6, 14). However, the identification of adult psychodid species by using morphological characters is difficult and can be misidentified (33). Whereas phylogenetic relationships and classification within the Psychodidae family is only known for the subfamily Phlebotominae, species-rich Pscyhodinae subfamily relationships with other species and within the family remains poorly understood (18). At present, studies on the clasification of the Pscyhodinae subfamily are generally based on the morphology of all life stages (egg, larvae, and adult) and fossil species (3437). Hennig (34) and Azar et al. (35) suggested a clade Trichomyiinae+Sycoracinae+Horaiellinae to be the sister group of the Psychodinae based on the morphology of mainly fossil species.

With the development of molecular techniques, the PCR technique, which mainly targets the nuclear and mitochondrial genes, has been most commonly used in molecular characterization and phylogenetic analyses of insect species in recent years (16, 17). The cytochrome b (cytb), mt-COI and mt-COII, NADH dehydrogenase subunit 1, and 28S and 16S ribosomal RNA gene regions were used to determine relationships within the subfamily Psychodinae in different region of the world (18). The molecular analyses of mitochondrial DNA have ensured diagnostic markers for the identification of species in many different insect groups. The mitochondrial-encoded genes, COI and COII, are among the more robust and reliable molecular markers for identification and phylogenetic analyses in most insect species because this gene region has highly conserved sequences and variable regions in vertebrates and insects (15-17, 38).

There have been no molecular-based studies conducted on moth flies in Turkey up to date, to the best of our knowledge. In this study, we describe the genotype characterization of moth flies by the DNA barcoding method based on mt-COI. We further determined phylogenetic relationships within the moth fly's specimens. Our results demonstrate that ERU-Telmatos3 and ERU-Telmatos6 isolates are grouped with T. albipunctatus isolates in India and Psychodidae sp. isolate in the United States. These species are located under the A1 haplogroup with a high bootstrap support (100%) and posterior probability (1.00) (Figure 2). According to the sequence BLAST analyses, the mean genetic distance between the A1 haplogroup and the A2 haplotype was 3.5[+ or -]0.8%.

Phylogenetic analyses revealed that the ERU-Psycho4 and ERU-Psycho5 isolates showed a 100% identity among the Psychodidae sp. isolates in Canada. The ERU-Psycho1 isolate within the B2 haplogroup was characterized as a new haplotype in this study. The genetic difference between the B2 haplogroup isolates and the ERU-Psycho1 isolates was calculated as 0.2[+ or -]0.2%. The mean genetic distance between the Diptera sp. isolate from the United States and Psychodidae sp. isolate from Canada within the B1 haplogroup and ERU-Psycho1 was 0.5[+ or -]0.2%. However, high genetic diversity (5.6[+ or -]1.0%) was found between the groups A and B. There are a limited number of studies on the phylogenetic relationship of the Psychodinae subfamily based on the mt-COI gene region in all world (18, 32). Espindola et al. (18) examined phylogenetic relationships among 52 Palearctic taxa of Psychodinae based on the mitochondrial DNA sequence. They report monophyly of the subfamily Psychodinae, and they found Psychodini samples in Clade II and also Psychoda comprised in several subclades of Clade II. Mokhtar et al. (32) found larvae in a 41-year-old female patient's feces in Malaysia. They were examinining the larval specimen under a stereomicroscope and identifed as a Psychodid larva. Then the COI gene region by DNA barcoding of larvae was amplified using primer pairs, and the DNA barcode from the specimen suggested that the specimen was the larval stage of C. albipunctatus.

CONCLUSION

Our study provided the first set of data on the molecular characterization and phylogeny of moth flies based on the DNA barcoding in Turkey. We provide an understanding of phylogenetic reconstruction of these species to determine the vectorial potentiality and epidemiology of moth flies in Turkey, and thus the results of our analyses may be fruitful in future research. Furthermore, this study may be helpful to determine proper pest management practices against the moth flies.

Ethics Committee Approval: Due to the material composed from insect specimens Ethics Committee Approval was not needed for this study.

Informed Consent: Not required in this study.

Peer-review: Externally peer-reviewed.

Author Contributions: Concept - Z.O., A.I., A.Y.; Design - Z.O., A.I., A.Y., O.D., A.C.; Supervision - Z.O., A.I., A.Y.; Funding - Z.O., A.I., A.Y.; Materials - Z.O., A.I., A.Y.; Data Collection and/or Processing - Z.O., A.I., A.Y., O.D., A.C.; Analysis and/or Interpretation - Z.O., A.I., A.Y.; Literature Review - Z.O., A.I.., A.Y., O.D., A.C.; Writing - Z.O., A.I., A.Y.; Critical Review - Z.O., A.I., A.Y.

Conflict of Interest: Authors have no conflicts of interest to declare.

Financial Disclosure: The authors declared that this study has received no financial support.

Etik Komite Onayi: Calisma materyalini insektler olusturdugundan etik komite onayi alinmamistir.

Hasta Onami: Bu calisma icin hasta onamina gerek yoktur.

Peer-review: Externally peer-reviewed.

Yazar Katkilari: Fikir - Z.O., A.I., A.Y.; Tasarim - Z.O., A.I., A.Y., O.D., A.C.; Denetleme - Z.O., A.I., A.Y.; Kaynaklar - Z.O., A.I., A.Y.; Malzemeler - Z.O., A.I., A.Y.; Veri toplanmasive/veya islemesi - Z.O., A.I., A.Y., O.D., A.C.; Analiz ve/veya yorum - Z.O., A.I., A.Y.; Literatur taramasi - Z.O., A.I., A.Y., O.D., A.C.; Yaziyi yazan - Z.O., A.I., A.Y.; Elestirel Inceleme - Z.O., A.I., A.Y.

Cikar Catismasi: Yazarlar cikar catismasi bildirmemislerdir.

Finansal Destek: Yazarlar bu calisma icin finansal destek almadiklarini beyan etmislerdir.

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Zuhal Onder [iD], Abdullah Inci [iD], Alparslan Yildirim [iD], Arif Ciloglu [iD], Onder Duzlu [iD]

Department of Parasitology, Erciyes University School of Medicine, Kayseri, Turkey

Address for Correspondence / Yazisma Adresi: Zuhal Onder E.mail: zuhalbiskin@erciyes.edu.tr

Received: 16.03.2018

Accepted: 03.05.2018

Gelis Tarihi: 16.03.2018

Kabul Tarihi: 03.05.2018

DOI: 10.5152/tpd.2018.5943
Table 1. Species used from Genbank for sequence alignment

Genbank Accession No   Species

AB907184               Telmatoscopus albipunctatus
HQ979025               Psychodidae sp.
KY924867               Telmatoscopus albipunctatus
KY924868               Telmatoscopus albipunctatus
KX054540               Psychodidae sp.
KX054541               Psychodidae sp.
HQ978770               Diptera sp.
KR992085               Psychodidae gen. PschodididGC sp.
KR988152               Psychodidae gen. PschodididGC sp.
KR990808               Psychodidae gen. PschodididGC sp. 1
KY924855               Psychodidae sp.
KY924866               Psychodidae sp.
KR990235               Psychodidae gen. PschodididGC sp.
KR770724               Psychodidae gen. PschodididGC sp.
KR722204               Psychodidae gen. PschodididGC sp.
KY924864               Psychodidae sp.

Genbank Accession No   Isolate           Origin

AB907184               COI13             India
HQ979025               BOLD:AAF9305      USA
KY924867               ERU-Telmatos3     Kayseri, Turkey
KY924868               ERU-Telmatos3     Kayseri, Turkey
KX054540               sc_05918          French Polynesia
KX054541               sc_05919          French Polynesia
HQ978770               BOLD:AAE5173      Canada
KR992085               BOLD-2016         Canada
KR988152               BOLD-2016         Canada
KR990808               BOLD-2016         Canada
KY924855               ERU-Psycho4       Kayseri, Turkey
KY924866               ERU-Psycho5       Kayseri, Turkey
KR990235               BOLD-2016         Canada
KR770724               BOLD-2016         Canada
KR722204               BOLD-2016         Canada
KY924864               ERU-Psycho1       Kayseri, Turkey
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Title Annotation:Ozgun Arastirma/Original Investigation
Author:Onder, Zuhal; Inci, Abdullah; Yildirim, Alparslan; Ciloglu, Arif; Duzlu, Onder
Publication:Turkish Journal of Parasitology
Article Type:Report
Date:Sep 1, 2018
Words:3844
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