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Predominance of Wolbachia Endosymbiont in the Microbiota Across Life MARK Stages of Bactrocera Latifrons (Insecta: Tephritidae)

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Predominance of Wolbachia Endosymbiont in the Microbiota Across Life MARK Stages of Bactrocera Latifrons (Insecta: Tephritidae) Meta Gene 14 (2017) 6–11 Contents lists available at ScienceDirect Meta Gene journal homepage: www.elsevier.com/locate/mgene Predominance of Wolbachia endosymbiont in the microbiota across life MARK stages of Bactrocera latifrons (Insecta: Tephritidae) ⁎ Hoi-Sen Yonga, Sze-Looi Songb, , Kah-Ooi Chuaa, Phaik-Eem Limb a Institute of Biological Sciences, University of Malaya, 50603 Kuala Lumpur, Malaysia b Institute of Ocean and Earth Sciences, University of Malaya, 50603 Kuala Lumpur, Malaysia ARTICLE INFO ABSTRACT Keywords: The Solanum fruit fly Bactrocera latifrons is an important agricultural pest. There is no report on the microbiota Bactrocera latifrons associated with this fruit fly. This study reports the bacterial communities associated with the life stages of this Wolbachia endosymbiont fruit fly from Malaysia. Illumina MiSeq next-generation sequencing of PCR-generated amplicons of 16S rRNA Microbiota gene revealed the presence of different number of bacterial OTUs in the life stages studied. The number of Next-generation sequencing bacterial OTUs at different taxonomic levels in the larva sample was much higher than in the adult male and adult female samples. The class Alphaproteobacteria of phylum Proteobacteria was predominant across the life stages studied (98.64% in the larva sample, 98.53% in pupa, 97.66% in adult male, and 99.89% in adult female). At the specific level, Wolbachia endosymbiont of Culex quinquefasciatus Pel was detected in all the life stages studied – 98.61% in the larva sample, 98.18% in pupa, 97.59% in adult male, and 99.88% in adult female. The ubiquitous presence of Wolbachia infections across life stages provides evidence for transmission from the larva stage to emerging adults. The role(s) of Wolbachia in B. latifrons remain to be determined. 1. Introduction The microbiota associated with Bactrocera fruit flies have been re- ported for B. cacuminata (Thaochan et al., 2010; Morrow et al., 2015b), The Solanum fruit fly Bactrocera latifrons (Hendel) is among the eco- B. carambolae (Yong et al., 2017), B. dorsalis (Andongma et al., 2015; nomically important species belonging to the Dacinae subfamily of tephritid Wang et al., 2011; Shi et al., 2012; Wang et al., 2013; Thaochan et al., fruit flies (Vargas et al., 2015). It is of primarily Asian distribution (Carroll 2013; Pramanik et al., 2014; Yong et al., 2017), B. jarvisi (Morrow et al., et al., 2002). Its range has however expanded through introductions into 2015b), B. neohumeralis (Morrow et al., 2015b), B. minax (Wang et al., Hawaii (Vargas and Nishida, 1985), Japan (Ishida et al., 2005), Tanzania 2014), B. oleae (Kounatidis et al., 2009; Ben-Yosef et al., 2010), B. tryoni (Mwatawala et al., 2010) and Kenya (De Meyer et al., 2011). A total of 59 (Thaochan et al., 2010; Morrow et al., 2015b), and B. zonata (Reddy plant species from 14 plant families are identified as hosts of B. latifrons, et al., 2014). As far as we are aware, there are no reports on B. latifrons. based on reported field infestation data (McQuate and Liquido, 2013). We report here the composition and diversity of bacteria associated However, it infests mainly solanaceous fruits (Yong et al., 2013; Vargas with the life stages of this fruit fly. MiSeq next-generation sequencing of et al., 2015). The adult male flies are not attracted to methyl eugenol or PCR-generated amplicons of 16S rRNA gene reveals predominance of Cue lure. Wolbachia endosymbionts in all the life stages studied. Fruit flies of the genus Bactrocera (and other tephritids) have been re- ported to harbor a great diversity of microbiota. In earlier studies, the gut 2. Materials and methods microbiota of Bactrocera fruit flies has been determined by culture-depen- dent and culture-independent methods. The Analytical Profile Index (API) 2.1. Ethics statement 20E system identifies only culturable bacteria (Thaochan et al., 2010). Molecular techniques reveal both culturable and unculturable species B. latifrons is an insect pest. It is not endangered or protected by law. (Thaochan et al., 2010). Recently, the microbiota associated with Bactrocera No permits are required to study this fruit fly. fruit flies have been studied by next-generation sequencing of PCR-gener- ated amplicons of the 16S rRNA gene (Wang et al., 2014; Andongma et al., 2015; Morrow et al., 2015b; Yong et al., 2017). ⁎ Corresponding author. E-mail address: [email protected] (S.-L. Song). http://dx.doi.org/10.1016/j.mgene.2017.07.007 Received 29 May 2017; Received in revised form 18 July 2017; Accepted 24 July 2017 Available online 26 July 2017 2214-5400/ © 2017 Elsevier B.V. All rights reserved. H.-S. Yong et al. Meta Gene 14 (2017) 6–11 2.2. Sample collection samples) including Shannon and Simpson indexes, Chao1, PD whole tree and Good's coverage were analysed based on sample sizes nor- Ripe chillies (Capsicum annuum) were collected from the garden of malised to the minimum number of sequences obtained among samples. University of Malaya and brought to the laboratory for observation Beta diversity (microbial diversity between samples) across the four (Yong et al., 2013). They were placed in screened containers with samples was calculated based upon Bray-Curtis dissimilarity matrix. suitable substrate for the larvae to develop and pupate (Yong, 1994). Principal Coordinate Analysis (PCoA) plot was constructed showing the Third instar larva upon emergence and pupa within a day after pupa- overall dissimilarity of bacterial community in different life stages. A tion were collected, rinsed and preserved in absolute ethanol. Pupae heatmap with OTU abundance and hierarchical clustering of samples were also collected and placed in plastic tubes for development. was generated using R version 3.2.4 with Euclidean distances specified Emerging adult flies were collected, sexed and preserved in absolute (Khang et al., 2016). ethanol. The specimens were stored in deep freezer until used. 3. Results 2.3. DNA extraction 3.1. 16S rDNA sequence reads A G-spin™ Total DNA Extraction Mini Kit (iNtRON Biotechnology, Inc., Korea) was used to extract the DNA of whole individual specimens The sequencing generated the following number of raw sequence of different development stages according to the manufacturer's in- reads: larva, 1,624,900; pupa, 1,743,328; adult male, 1,397,006; and structions with minor modifications – the incubation time of lysate was adult female, 1,362,604. After quality filtering, the number of sequence prolonged to one hour to ensure complete lysis of the fruit fly sample. reads were: larva, 175,502; pupa, 199,168; adult male, 137,191; and adult female, 167,470. The number of reads varied among the life 2.4. PCR amplification and next generation sequencing stages. Rarefaction analysis revealed that the OTU count in these samples increased sharply before attaining a plateau (Fig. 1). Polymerase chain reaction (PCR) was performed with KAPA HiFi HotStart ReadyMix PCR Kit (KAPA BioSystems, USA) containing 3.2. Bacterial composition 2 × KAPA HiFi HotStart DNA Polymerase, 1 μMofeachprimerand5ng/ μL DNA to a total volume of 25 μL. The hypervariable V3-V4 MiSeq next-generation sequencing of PCR-generated amplicons of region of the bacterial 16S rRNA gene sequences were amplified with 16S rRNA gene revealed the presence of different number of bacterial primer pair MiSeq341F (5′-TCGTCGGCAGCGTCAGATGTGTATAAGA OTUs in the life stages studied (Table 1). The number of bacterial OTUs GACAGCCTACGGGNGGCWGCAG-3′) and MiSeq805R (5′-GTCTCGTGG at different taxonomic levels in the larva sample was much higher than GCTCGGAGATGTGTATAAGAGACAGGACTACHVGGGTATCTAATCC-3′). in the adult male and adult female samples (Table 1). Five phyla were The 5′-ends are Illumina adapter sequences while the 3′-ends of the pri- detected in the larva sample versus two in adult male and four in adult mers amplify the V3-V4 region of the 16S rRNA gene (Klindworth et al., female. At the species level, 71 OTUs were present in the larva sample 2013). The parameters for PCR amplification were as described in 16S versus 24 in adult male and 11 in adult female. The number of OTUs at Metagenomic Sequencing Library Preparation protocol: 3 min denatura- the family, genus and species level for the adult male sample was higher tionstepat95°C,followedby25cyclesof30sat95°C,30sat55°C,30s than the adult female, particularly at the lower taxonomic levels elongation at 72 °C, and a final extension at 72 °C for 5 min. PCR products (Table 1). were purified using Agencourt AMPure XP kit (Beckman Coulter, Brea, Two phyla (Firmicutes and Proteobacteria) were present in all the life CA, USA). Purified amplicons were barcoded using the Nextera XT Index stages, while three additional phyla (Actinobacteria, Bacteroidetes, and Kit and were purified again before quantification. Size estimation of the Cyanobacteria/Melainabacteria group) occurred in the larval and pupal library was carried out on a 2100 Bioanalyzer using High Sensitivity DNA stages but absent in the adult male (Table 2). Actinobacteria and Bac- Analysis Kit (Agilent Technologies). Quantitative real-time PCR for library teroidetes occurred at very low relative frequency in the adult female. A quantification was conducted using KAPA Library Quantification Kit for small proportion of reads was unassigned. Proteobacteria was the pre- Illumina sequencing platforms (KAPA Biosystems, Boston, MA, USA) on dominant phylum across the life stages studied (98.94% in the larva Eco Real-Time PCR System. Sequencing was performed using the Illumina sample, 99.92% in pupa, 99.98% in adult male, and 99.99% in adult MiSeq System (2 × 250 bp paired-end reads) (Illumina, USA). female) (Table 2). It was represented by 3 classes: (i) the predominant class Alphaproteobacteria (98.64% in the larva sample, 98.53% in pupa, 2.5. Bioinformatics and statistical analysis 97.66% in adult male, and 99.89% in adult female); (ii) Betaproteo- bacteria with very low relative abundance in the larva (0.02%), pupa Demultiplexed raw sequences were extracted from the Illumina (0.00%) and adult male (0.00%); and (iii) Gammaproteobacteria with MiSeq system in FASTQ format and the quality of sequences was the adult male sample (2.32%) having a higher relative abundance than evaluated using the FastQC software (Andrews, 2010).
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