Diet and irradiation effects on the bacterial community composition and structure in the gut of domesticated teneral and mature Queensland fruit fly, Bactrocera tryoni (Diptera: Tephritidae)

Abstract Background Mass-rearing, domestication and gamma irradiation of tephritid fruit flies used in sterile insect technique (SIT) programmes can negatively impact fly quality and performance. Symbiotic bacteria supplied as probiotics to mass-reared fruit flies may help to overcome some of these...

Full description

Bibliographic Details
Main Authors: Deane N. Woruba, Jennifer L. Morrow, Olivia L. Reynolds, Toni A. Chapman, Damian P. Collins, Markus Riegler
Format: Article
Language:English
Published: BMC 2019-12-01
Series:BMC Microbiology
Subjects:
Online Access:https://doi.org/10.1186/s12866-019-1649-6
id doaj-4511546a9fe1493b86ec18c536ab4f6b
record_format Article
spelling doaj-4511546a9fe1493b86ec18c536ab4f6b2020-12-27T12:07:45ZengBMCBMC Microbiology1471-21802019-12-0119S111310.1186/s12866-019-1649-6Diet and irradiation effects on the bacterial community composition and structure in the gut of domesticated teneral and mature Queensland fruit fly, Bactrocera tryoni (Diptera: Tephritidae)Deane N. Woruba0Jennifer L. Morrow1Olivia L. Reynolds2Toni A. Chapman3Damian P. Collins4Markus Riegler5Plant Biosecurity Cooperative Research CentreHawkesbury Institute for the Environment, Western Sydney UniversityPlant Biosecurity Cooperative Research CentrePlant Biosecurity Cooperative Research CentreBiometrics Unit, NSW Department of Primary Industries, Elizabeth Macarthur Agricultural InstituteHawkesbury Institute for the Environment, Western Sydney UniversityAbstract Background Mass-rearing, domestication and gamma irradiation of tephritid fruit flies used in sterile insect technique (SIT) programmes can negatively impact fly quality and performance. Symbiotic bacteria supplied as probiotics to mass-reared fruit flies may help to overcome some of these issues. However, the effects of tephritid ontogeny, sex, diet and irradiation on their microbiota are not well known. Results We have used next-generation sequencing to characterise the bacterial community composition and structure within Queensland fruit fly, Bactrocera tryoni (Froggatt), by generating 16S rRNA gene amplicon libraries derived from the guts of 58 individual teneral and mature, female and male, sterile and fertile adult flies reared on artificial larval diets in a laboratory or mass-rearing environment, and fed either a full adult diet (i.e. sugar and yeast hydrolysate) or a sugar only adult diet. Overall, the amplicon sequence read volume in tenerals was low and smaller than in mature adult flies. Operational taxonomic units (OTUs), belonging to the families Enterobacteriaceae (8 OTUs) and Acetobacteraceae (1 OTU) were most prevalent. Enterobacteriaceae dominated laboratory-reared tenerals from a colony fed a carrot-based larval diet, while Acetobacteraceae dominated mass-reared tenerals from a production facility colony fed a lucerne chaff based larval diet. As adult flies matured, Enterobacteriaceae became dominant irrespective of larval origin. The inclusion of yeast in the adult diet strengthened this shift away from Acetobacteraceae towards Enterobacteriaceae. Interestingly, irradiation increased 16S rRNA gene sequence read volume. Conclusions Our findings suggest that bacterial populations in fruit flies experience significant bottlenecks during metamorphosis. Gut bacteria in teneral flies were less abundant and less diverse, and impacted by colony origin. In contrast, mature adult flies had selectively increased abundances for some gut bacteria, or acquired these bacteria from the adult diet and environment. Furthermore, irradiation augmented bacterial abundance in mature flies. This implies that either some gut bacteria were compensating for damage caused by irradiation or irradiated flies had lost their ability to regulate bacterial load. Our findings suggest that the adult stage prior to sexual maturity may be ideal to target for probiotic manipulation of fly microbiota to increase fly performance in SIT programmes.https://doi.org/10.1186/s12866-019-1649-6Sterile insect techniquemicrobiome16S rRNA geneEnterobacteriaceaeAcetobacteraceaeAsaia sp.
collection DOAJ
language English
format Article
sources DOAJ
author Deane N. Woruba
Jennifer L. Morrow
Olivia L. Reynolds
Toni A. Chapman
Damian P. Collins
Markus Riegler
spellingShingle Deane N. Woruba
Jennifer L. Morrow
Olivia L. Reynolds
Toni A. Chapman
Damian P. Collins
Markus Riegler
Diet and irradiation effects on the bacterial community composition and structure in the gut of domesticated teneral and mature Queensland fruit fly, Bactrocera tryoni (Diptera: Tephritidae)
BMC Microbiology
Sterile insect technique
microbiome
16S rRNA gene
Enterobacteriaceae
Acetobacteraceae
Asaia sp.
author_facet Deane N. Woruba
Jennifer L. Morrow
Olivia L. Reynolds
Toni A. Chapman
Damian P. Collins
Markus Riegler
author_sort Deane N. Woruba
title Diet and irradiation effects on the bacterial community composition and structure in the gut of domesticated teneral and mature Queensland fruit fly, Bactrocera tryoni (Diptera: Tephritidae)
title_short Diet and irradiation effects on the bacterial community composition and structure in the gut of domesticated teneral and mature Queensland fruit fly, Bactrocera tryoni (Diptera: Tephritidae)
title_full Diet and irradiation effects on the bacterial community composition and structure in the gut of domesticated teneral and mature Queensland fruit fly, Bactrocera tryoni (Diptera: Tephritidae)
title_fullStr Diet and irradiation effects on the bacterial community composition and structure in the gut of domesticated teneral and mature Queensland fruit fly, Bactrocera tryoni (Diptera: Tephritidae)
title_full_unstemmed Diet and irradiation effects on the bacterial community composition and structure in the gut of domesticated teneral and mature Queensland fruit fly, Bactrocera tryoni (Diptera: Tephritidae)
title_sort diet and irradiation effects on the bacterial community composition and structure in the gut of domesticated teneral and mature queensland fruit fly, bactrocera tryoni (diptera: tephritidae)
publisher BMC
series BMC Microbiology
issn 1471-2180
publishDate 2019-12-01
description Abstract Background Mass-rearing, domestication and gamma irradiation of tephritid fruit flies used in sterile insect technique (SIT) programmes can negatively impact fly quality and performance. Symbiotic bacteria supplied as probiotics to mass-reared fruit flies may help to overcome some of these issues. However, the effects of tephritid ontogeny, sex, diet and irradiation on their microbiota are not well known. Results We have used next-generation sequencing to characterise the bacterial community composition and structure within Queensland fruit fly, Bactrocera tryoni (Froggatt), by generating 16S rRNA gene amplicon libraries derived from the guts of 58 individual teneral and mature, female and male, sterile and fertile adult flies reared on artificial larval diets in a laboratory or mass-rearing environment, and fed either a full adult diet (i.e. sugar and yeast hydrolysate) or a sugar only adult diet. Overall, the amplicon sequence read volume in tenerals was low and smaller than in mature adult flies. Operational taxonomic units (OTUs), belonging to the families Enterobacteriaceae (8 OTUs) and Acetobacteraceae (1 OTU) were most prevalent. Enterobacteriaceae dominated laboratory-reared tenerals from a colony fed a carrot-based larval diet, while Acetobacteraceae dominated mass-reared tenerals from a production facility colony fed a lucerne chaff based larval diet. As adult flies matured, Enterobacteriaceae became dominant irrespective of larval origin. The inclusion of yeast in the adult diet strengthened this shift away from Acetobacteraceae towards Enterobacteriaceae. Interestingly, irradiation increased 16S rRNA gene sequence read volume. Conclusions Our findings suggest that bacterial populations in fruit flies experience significant bottlenecks during metamorphosis. Gut bacteria in teneral flies were less abundant and less diverse, and impacted by colony origin. In contrast, mature adult flies had selectively increased abundances for some gut bacteria, or acquired these bacteria from the adult diet and environment. Furthermore, irradiation augmented bacterial abundance in mature flies. This implies that either some gut bacteria were compensating for damage caused by irradiation or irradiated flies had lost their ability to regulate bacterial load. Our findings suggest that the adult stage prior to sexual maturity may be ideal to target for probiotic manipulation of fly microbiota to increase fly performance in SIT programmes.
topic Sterile insect technique
microbiome
16S rRNA gene
Enterobacteriaceae
Acetobacteraceae
Asaia sp.
url https://doi.org/10.1186/s12866-019-1649-6
work_keys_str_mv AT deanenworuba dietandirradiationeffectsonthebacterialcommunitycompositionandstructureinthegutofdomesticatedteneralandmaturequeenslandfruitflybactroceratryonidipteratephritidae
AT jenniferlmorrow dietandirradiationeffectsonthebacterialcommunitycompositionandstructureinthegutofdomesticatedteneralandmaturequeenslandfruitflybactroceratryonidipteratephritidae
AT olivialreynolds dietandirradiationeffectsonthebacterialcommunitycompositionandstructureinthegutofdomesticatedteneralandmaturequeenslandfruitflybactroceratryonidipteratephritidae
AT toniachapman dietandirradiationeffectsonthebacterialcommunitycompositionandstructureinthegutofdomesticatedteneralandmaturequeenslandfruitflybactroceratryonidipteratephritidae
AT damianpcollins dietandirradiationeffectsonthebacterialcommunitycompositionandstructureinthegutofdomesticatedteneralandmaturequeenslandfruitflybactroceratryonidipteratephritidae
AT markusriegler dietandirradiationeffectsonthebacterialcommunitycompositionandstructureinthegutofdomesticatedteneralandmaturequeenslandfruitflybactroceratryonidipteratephritidae
_version_ 1724369378933211136