Beyond canonical models: why a broader understanding of Diptera-microbiota interactions is essential for vector-borne disease control

Arellano, Aldo A.; Sommer, Andrew J.; Coon, Kerri L.

doi:10.1007/s10682-022-10197-2

Cited by 6 publications

(6 citation statements)

References 208 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Future work will elucidate the role of biting flies in the transmission of not only bovine mastitis pathogens, but other farm-associated zoonotic pathogens including E. coli O157, Brucella , and Salmonella (Ruegg et al, 2003; Seleem et al, 2010). Future work will also leverage these results to provide novel insights into the ecology and evolution of these and other dipteran insects more broadly, including species that serve important roles as bioindicators, biocontrol agents, sources of nutrition for other organisms, and/or nuisance pests, as well as other vectors of disease (Arellano et al, 2023).…”

Section: Discussionmentioning

confidence: 99%

Stable flies are bonafide reservoirs of mastitis-associated bacteria

Sommer,

Kettner,

Coon

2024

Preprint

Self Cite

View full text Add to dashboard Cite

HematophagousStomoxys(stable) fly populations in dairy barns are sustained by a constant availability of cattle hosts and manure, which serve as major reservoirs of both zoonotic and opportunistic bacterial pathogens. However, the overall composition and diversity of bacterial communities associated withStomoxysflies and the ability of biting flies to acquire and transmit potentially pathogenic bacteria present in their surrounding environment remain to be investigated. Here, we present the first culture-independent examination ofStomoxys-associated bacterial communities through longitudinal sampling of fly and manure samples collected from two connected dairy facilities in South Central Wisconsin. High throughput 16S rRNA gene amplicon sequencing was used to characterize and compare bacterial communities present on or within flies and in manure collected from the same facility. Bacterial alpha diversity was overall higher in manure samples as compared to fly samples, with manure-associated bacterial communities being dominated by members of the Bacteroidales, Eubacteriales, and Oscillospirales. In contrast, flies harbored relatively low-complexity communities dominated by members of the Enterobacterales, Staphylococcales, and Lactobacillales. Clinically relevant bacterial strains, includingEscherichiaspp. and other taxa associated with mastitic cows housed in the same facilities, were detected in paired fly and manure samples but exhibited dramatically elevated abundances in fly samples as compared to manure samples. Viable colonies ofEscherichia,Klebsiella, andStaphylococcusspp. were also readily isolated from fly samples, confirming that flies harbor culturable mastitis associated bacteria. This study provides definitive support for a potential role for biting flies in mediating bacterial pathogen transmission in dairy barns and other agricultural settings.IMPORTANCEDisease prevention on dairy farms has significant implications for cattle health, food security, and zoonosis. Of particular importance is the control of bovine mastitis, which can be caused by a diverse array of environmental bacterial pathogens, includingKlebsiella,E. coli,Streptococcus, andStaphylococcusspp. Despite being one of the most significant and costly cattle diseases worldwide, the epidemiology of bovine mastitis is not well understood. This study provides the first culture-dependent and culture-independent evidence to support the potential for biting flies to transmit opportunistic bovine and human pathogens in agricultural settings. It also links carriage of specific bacterial taxa in flies to clinical mastitis cases in cows housed in the same facility at the time of sampling. Altogether, these results indicate that biting flies represent an important, yet understudied biosecurity threat to animal husbandry facilities.

show abstract

Section: Discussionmentioning

confidence: 99%

Stable flies are bonafide reservoirs of mastitis-associated bacteria

Sommer,

Kettner,

Coon

2024

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…Despite differences in alpha and beta diversity, the vast majority of bacteria in fly samples could be traced to their corresponding manure samples, suggesting that, like other dipteran insects including mosquitoes, Stomoxys flies acquire their microbiota from the environments in which they breed (summarized in references 56 – 58 ). However, while our results support that flies visit manure and externally acquire bacteria, whether the internal adult microbiota is primarily shaped by adult feeding activities or transstadial transmission of bacteria from larvae, which develop in manure, is currently unknown.…”

Section: Discussionmentioning

confidence: 99%

“…This decision was driven in large part by the methodology used to collect flies in this study, which made explanting the gut with no possibility of contamination difficult. However, prior studies in related muscid flies and other dipteran insects have experimentally demonstrated that multiple species contain no bacteria as larvae before hatching from eggs, but rapidly acquire a gut microbiota from the environment in which they hatch by feeding (summarized in references 56 , 57 ). This, combined with the fact that (i) almost all of the reads present in our surface-sterilized internal fly samples represented ASVs that were present in manure samples collected from the same facility on the same sampling date, and (ii) viable colonies of commonly shared taxa were readily isolated from internal fly samples, strongly suggests that most of the bacteria we identified in adult Stomoxys flies in the current study are gut community members.…”

Section: Discussionmentioning

confidence: 99%

Stable flies are bona fide carriers of mastitis-associated bacteria

Sommer,

Kettner,

Coon

2024

mSphere

Self Cite

View full text Add to dashboard Cite

Hematophagous Stomoxys (stable) fly populations in dairy barns are sustained by a constant availability of cattle hosts and manure, which serve as major reservoirs of both zoonotic and opportunistic bacterial pathogens. However, the composition of the Stomoxys fly microbiota, the mechanisms by which flies acquire their microbiome, and the ability of potentially pathogenic bacteria to colonize and persist in fly hosts remain to be investigated. Here, we longitudinally collected fly and manure samples from two connected dairy facilities. High throughput 16S rRNA gene amplicon sequencing was then used to characterize and compare bacterial communities present on or within flies and in manure collected from the same facility, while culture-dependent methods were used to verify the viability of clinically relevant bacteria. Bacterial alpha diversity was overall higher in manure samples as compared to fly samples, with manure-associated bacterial communities being dominated by members of the Bacteroidales, Eubacteriales, and Oscillospirales. In contrast, flies harbored relatively low-complexity communities dominated by members of the Enterobacterales, Staphylococcales, and Lactobacillales. Clinically relevant bacterial strains, including Escherichia spp. and other taxa associated with mastitic cows housed in the same facilities, were detected in paired fly and manure samples but exhibited dramatically elevated abundances in fly samples as compared to manure samples. Viable colonies of Escherichia , Klebsiella , and Staphylococcus spp. were also readily isolated from fly samples, confirming that flies harbor culturable mastitis-associated bacteria. This study identifies biting flies as bona fide carriers of opportunistically pathogenic bacterial taxa on dairy farms. IMPORTANCE Disease prevention on dairy farms has significant implications for cattle health, food security, and zoonosis. Of particular importance is the control of bovine mastitis, which can be caused by diverse bacteria, including Klebsiella , Escherichia coli , Streptococcus , and Staphylococcus spp. Despite being one of the most significant and costly cattle diseases worldwide, the epidemiology of bovine mastitis is not well understood. This study provides parallel culture-independent and culture-dependent evidence to support the carriage of opportunistically pathogenic bacteria by Stomoxys flies on dairy farms. We further show that the fly microbiota is enriched in clinically relevant taxa—the vast majority of which can be traced to the manure habitats in which flies breed. Altogether, our results identify biting flies as underrecognized carriers of bacterial taxa associated with environmental bovine mastitis and other opportunistic infections in vertebrates and offer important insights into mechanisms of microbial acquisition by these and other medically important insects.

show abstract

“…However, in the context of exponentially growing volumes of scientific literature on genetic diversity of mosquito larval gut microbiota and its association with diverse phenotypic consequences, it is quite surprising that information available on mechanism of mosquito-gut microbiota association is extremely scanty. Considering the accumulating evidence on the role of gut microbiota in development, reproduction, fecundity, vectorial capacity etc., elucidation of functional significance of mosquito-gut microbiota interaction in larval physiology and metabolism are essential for controlled manipulation of microbiota as a potential vector-control strategy (Arellano et al, 2023; Gomez et al, 2022; Cansado-Utrilla et al, 2021; Gao et al, 2020; Huang et al, 2020; Scolari et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

“…Considering the accumulating evidence on the role of larval gut microbiota in nutrition, growth, development, and their carryover effects (in reproduction, fecundity, vector competence etc.) during the subsequent adult stages, elucidation of functional significance of mosquito-gut microbiota interaction in larval physiology and metabolism are essential for controlled manipulation of gut associated microbiota as a potential strategy for vector-control (Harrison et al, 2023; Arellano et al, 2023; Giraud et al, 2022; Gomez et al, 2022; Cansado-Utrilla et al, 2021; Gao et al, 2020; Huang et al, 2020; Scolari et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Select Gut Bacteria Promote Mosquito Larval Growth by Contributing Protease Activity and Optimal Ionic Microenvironment for Protein Digestion

Samanta,

Datta

2024

Preprint

View full text Add to dashboard Cite

Mosquitoes are known to harbor a highly functional gut microbiota, which strongly influence its vector competence through regulating nutrition, development, immunity, fecundity, reproduction, resistance to insecticides, etc. Therefore, a thorough understanding of the function of gut microbiota is required to develop novel and more effective vector-control tactics. With an aim to investigating the role of gut associated bacteria in the larval physiology, we conducted experiments using axenic and gnotobiotic larvae of Aedes albopictus. Our results show that gut associated bacteria along with an intact Carbonic Anhydrase (CA) activity is essential for establishment and maintenance of the characteristic gut pH profile of larvae, which in turn is essential for its digestion. Further, we documented that the requirement of ‘live’ bacteria for establishment of gut pH profile cannot be replaced by either bacterial cell-free supernatant or lysate. Interestingly, we observed that not all the members the gut microbiome has the capability to establish gut pH profile, suggesting that different members of the microbiome possibly have different roles in the larval physiology. Our findings thus reveal an important mechanism through which bacteria modulate different phenotypes in mosquito, which in turn impacts their life-history traits.

show abstract

Beyond canonical models: why a broader understanding of Diptera-microbiota interactions is essential for vector-borne disease control

Cited by 6 publications

References 208 publications

Stable flies are bonafide reservoirs of mastitis-associated bacteria

Stable flies are bonafide reservoirs of mastitis-associated bacteria

Stable flies are bona fide carriers of mastitis-associated bacteria

Select Gut Bacteria Promote Mosquito Larval Growth by Contributing Protease Activity and Optimal Ionic Microenvironment for Protein Digestion

Contact Info

Product

Resources

About