Honey Bee Larval and Adult Microbiome Life Stages Are Effectively Decoupled with Vertical Transmission Overcoming Early Life Perturbations

Kowallik, Vienna; Mikheyev, Alexander S.

doi:10.1128/mbio.02966-21

Cited by 27 publications

(20 citation statements)

References 113 publications

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“…E.g., a subsequent in-depth study of Australian viruses, where libraries were prepared and sequenced Australia, without the possibility of cross-contamination, failed to find DWV (43). To further illustrate this point, a cursory examination of sequenced negative controls in the NCBI SRA database (search terms negative control AND "Apis mellifera"[orgn] in RNA data, 19 January 2023), yielded just two sequencing runs of library blanks (44), though both have DWV contamination present (accession numbers DRR333172 and DRR333191). We recommend that future studies aiming to show the presence of DWV, sequence negative controls as standard practice to rule out contamination.…”

Section: Discussionmentioning

confidence: 99%

Evolutionarily diverse origins of honey bee deformed wing viruses

Hasegawa

Techer

al-Hissnawi

et al. 2023

Preprint

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Novel transmission routes can allow infectious diseases to spread, often with devastating consequences. Ectoparasitic varroa mites vector a diversity of RNA viruses and, having switched hosts from the eastern to western honey bees (Apis cerana to Apis mellifera). They provide an opportunity to explore how novel transmission routes shape disease epidemiology. As the principal driver of the spread of Deformed Wing Viruses (mainly DWV-A and DWV-B), varroa infestation has also driven global honey bee health declines. The more virulent DWV-B strain has been replacing the original DWV-A strain in many regions over the past two decades. Yet, how these viruses originated and spread remains poorly understood. Here we use a phylogeographic analysis based on whole genome data to reconstruct the origins and demography of DWV spread. We found that, rather than reemerging in western honey bees after varroa switched hosts, as suggested by previous work, DWV-A most likely originated in Asia and spread in the mid-20th century. It also showed a massive population size expansion following the varroa host switch. By contrast, DWV-B was most likely acquired more recently from a source outside Asia, and appears absent from eastern honey bees, the original varroa host. These results highlight the dynamic nature of viral adaptation, whereby a vector's host switch can give rise to competing and increasingly virulent disease pandemics. The evolutionary novelty and rapid global spread of these host-virus interactions, together with observed spillover into other species, illustrate how increasing globalisation poses urgent threats to biodiversity and food security.

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Section: Discussionmentioning

confidence: 99%

Evolutionarily diverse origins of honey bee deformed wing viruses

Hasegawa

Techer

al-Hissnawi

et al. 2023

Preprint

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“…Feeding macerated honey bee guts to other bees is an established method of microbial transfer in laboratory studies ( Powell et al, 2014 ; Zheng et al, 2018 ; Kowallik and Mikheyev, 2021 ). However, since bees do not defecate in captivity, toxins such as tetracycline could conceivably accumulate in the hindgut.…”

Section: Discussionmentioning

confidence: 99%

“…However, the aim was to provide enough time that the microbiome can be fully established. We previously experienced that when newly emerged bees receive a microbiome pool for 48 h, they show the full adult bee microbiome in composition and abundance after 7 days ( Kowallik and Mikheyev, 2021 ). It is also known that under natural conditions, adult bees get colonized within the first 2 days after emergence which is followed by rapid establishment within 4 to 6 days post-eclosion ( Powell et al, 2014 ).…”

Section: Methodsmentioning

confidence: 99%

“…The adult honey bee microbiome consists of ~8 bacterial phylotypes that are involved in key biological functions such as nutrition, digestion, and immunity ( Engel et al, 2016 ; Emery et al, 2017 ; Kešnerová et al, 2017 ; Raymann and Moran, 2018 ). Because young adults emerge from pupation without a microbiome, they can reliably be inoculated with a microbiome of choice in the lab ( Powell et al, 2014 ; Zheng et al, 2018 ; Kowallik and Mikheyev, 2021 ). Thus, it is possible to serially transfer microbiomes across worker ‘generations’ to study how microbial changes in response to environmental stressors affect host phenotypes and health.…”

Section: Introductionmentioning

confidence: 99%

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Experimental inheritance of antibiotic acquired dysbiosis affects host phenotypes across generations

2022

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Microbiomes can enhance the health, fitness and even evolutionary potential of their hosts. Many organisms propagate favorable microbiomes fully or partially via vertical transmission. In the long term, such co-propagation can lead to the evolution of specialized microbiomes and functional interdependencies with the host. However, microbiomes are vulnerable to environmental stressors, particularly anthropogenic disturbance such as antibiotics, resulting in dysbiosis. In cases where microbiome transmission occurs, a disrupted microbiome may then become a contagious pathology causing harm to the host across generations. We tested this hypothesis using the specialized socially transmitted gut microbiome of honey bees as a model system. By experimentally passaging tetracycline-treated microbiomes across worker ‘generations’ we found that an environmentally acquired dysbiotic phenotype is heritable. As expected, the antibiotic treatment disrupted the microbiome, eliminating several common and functionally important taxa and strains. When transmitted, the dysbiotic microbiome harmed the host in subsequent generations. Particularly, naïve bees receiving antibiotic-altered microbiomes died at higher rates when challenged with further antibiotic stress. Bees with inherited dysbiotic microbiomes showed alterations in gene expression linked to metabolism and immunity, among other pathways, suggesting effects on host physiology. These results indicate that there is a possibility that sublethal exposure to chemical stressors, such as antibiotics, may cause long-lasting changes to functional host-microbiome relationships, possibly weakening the host’s progeny in the face of future ecological challenges. Future studies under natural conditions would be important to examine the extent to which negative microbiome-mediated phenotypes could indeed be heritable and what role this may play in the ongoing loss of biodiversity.

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“…Through integration of statistics, machine learning and multi-omics technologies, we could solve the three challenges in complex fermentation processes through three research steps [28][29][30]. First, machine learning and prediction modelling can help calculate and classify whether abiotic or biotic factors cause unstable fermentation outcomes [31,32].…”

Section: Introductionmentioning

confidence: 99%

Regulating microbiome metabolic stability for stable indigenous liquor fermentation

Tan

Zhu

Wijffels

et al. 2023

Preprint

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Background Regulating microbial metabolic stability is an ever-challenging goal in the food industry to ensure the productivity and quality of fermented foods. The microbiome underlying traditional Chinese liquor fermentation is such a representative microbiome metabolism that is affected by many dynamic abiotic/biotic factors. The complex microbial activities bring beneficial qualities (complex and rich aroma profiles, etc.) to the fermented product, but can also cause unstable fermentation outcomes. Here, we designed a three-step experiment (abiotic regulation; biotic regulation; lab-scale validation) to explore which factors cause unstable fermentation outcomes and how to regulate microbiome metabolic functional stability accordingly. Results We found that 30.5% industrial fermentation of traditional Chinese liquor outcomes could be precisely predicted by initial abiotic factors. We could ensure the stability of partial fermentation batches by regulating the initial ratio of acidity to reducing sugar, moisture, and starch. Furthermore, in two representative unpredictable fermentation batches (named batch A and batch B), we found that unstable fermentation outcomes occurred even with similar initial abiotic factors after a dynamic three-phase fermentation. Unstable fermentation batches showed fluctuations in microbial community assembly that affected fermentation stability by altering the beneficial distribution (metabolic flux) of redundant metabolic pathways between yeasts and Lactobacilli. The metabolism of batch B was more stable than that of batch A due to the consistent overexpression of a specific set of bacterial metabolic genes. In repeated feed-batch fermentation processes, the difference in metabolic functional stability between the two batches was amplified 9.02 times. Batch B had significantly lower microbiome metabolic fluctuations than batch A, with higher robustness and lower complexity of the metabolic functional network. Moreover, we found that adjusting the initial microbial inoculation ratio could regulate both the metabolic beneficial distribution and temporal metabolic fluctuations of the microbiome to appropriately reduce the instability caused by biotic factors. Conclusions This study demonstrates that rationally regulating initial parameters and microbial inoculation ratio is a practical strategy to optimize indigenous liquor fermentation. The stable microbial beneficial distribution and high metabolic robustness are essential to obtain the ideal microbiome metabolic stability. Our study provides insights and shows the feasibility of enhancing metabolic functional stability through initial conditions in dynamic microbial ecosystems.

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Honey Bee Larval and Adult Microbiome Life Stages Are Effectively Decoupled with Vertical Transmission Overcoming Early Life Perturbations

Cited by 27 publications

References 113 publications

Evolutionarily diverse origins of honey bee deformed wing viruses

Evolutionarily diverse origins of honey bee deformed wing viruses

Experimental inheritance of antibiotic acquired dysbiosis affects host phenotypes across generations

Regulating microbiome metabolic stability for stable indigenous liquor fermentation

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