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Microorganisms
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Microorganisms in Pollinators: Interactions with Other Factors
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Microorganisms in Pollinators: Interactions with Other Factors

A special issue of Microorganisms (ISSN 2076-2607).

Deadline for manuscript submissions: closed (28 February 2021) | Viewed by 40921

Special Issue Editors

Dr. Raquel Martín Hernández

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Guest Editor
Honey Bee Health, Centro de Investigación Apícola y Agroambiental de Marchamalo (CIAPA), Instituto Regional de Investigación Agroalimentario y Forestal (IRIAF), Junta de Comunidades de Castilla –La Mancha, 19180 Marchamalo, Spain
Interests: honey bee health; microsporidia; Nosema; viruses; Fungi; bee microbiota; pathogen interaction
Special Issues, Collections and Topics in MDPI journals
Dr. Mariano Higes Pascual

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Guest Editor
Honey Bee Health, Centro de Investigación Apícola y Agroambiental de Marchamalo (CIAPA), Instituto Regional de Investigación Agroalimentario y Forestal (IRIAF), Junta de Comunidades de Castilla –La Mancha, 19180 Marchamalo, Spain
Interests: honey bee health; microsporidia; Nosema; viruses; Varroa; trypanosomatids; pesticide residues
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Pollinating insects are essential for maintaining wild and cultivated ecosystems. In fact, much of the world’s agricultural production depends on the activity of these insects. Honeybees are one of the most efficient pollinators since they form colonies of thousands of individuals and, also, because colonies can be moved for the pollination of certain crops or areas of interest as a result of beekeeping activity. However, there are many other species of wild bees (social or solitary) or insects that participate in pollination, some of them commercially exploited and, therefore, they are also crucial for the maintenance of plant and animal biodiversity. In recent years, a large loss of pollinators has been detected worldwide and many researchers have focused on studying the causes of this decrease. Pathogenic microorganisms including bacteria, fungi, and viruses that affect both the adult and immature stages have been proposed as the primary cause of this loss. However, pollinators live in a complex world in which a large number of interactions occur, not only among pathogens (including mites) or their microbiota, but also with host genetic and several abiotic factors (such as nutrition, pesticides, or climate change, among others). In this Special Issue, we plan to explore the relationships established among different microorganisms, pathogenic or otherwise, and how insect genetic or abiotic factors interact with the microorganism and in what way they influence pollinator health.

Dr. Raquel Martín Hernández
Dr. Mariano Higes Pascual
Guest Editors

Manuscript Submission Information

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Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Microorganisms is an international peer-reviewed open access monthly journal published by MDPI.

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Keywords

  • insect pollinators
  • honeybee
  • bumble bee
  • microsporidia
  • viruses
  • bacteria
  • health
  • interaction
  • nutrition influence on microorganism
  • pesticide influence on microorganism
  • genetic influence on microorganism

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Related Special Issue

Published Papers (9 papers)

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Research

12 pages, 1422 KiB  
Article
Intra-Colonial Viral Infections in Western Honey Bees (Apis Mellifera)
by Loreley Castelli, María Laura Genchi García, Anne Dalmon, Daniela Arredondo, Karina Antúnez, Ciro Invernizzi, Francisco José Reynaldi, Yves Le Conte and Alexis Beaurepaire
Microorganisms 2021, 9(5), 1087; https://doi.org/10.3390/microorganisms9051087 - 18 May 2021
Cited by 5 | Viewed by 3597
Abstract
RNA viruses play a significant role in the current high losses of pollinators. Although many studies have focused on the epidemiology of western honey bee (Apis mellifera) viruses at the colony level, the dynamics of virus infection within colonies remains poorly [...] Read more.
RNA viruses play a significant role in the current high losses of pollinators. Although many studies have focused on the epidemiology of western honey bee (Apis mellifera) viruses at the colony level, the dynamics of virus infection within colonies remains poorly explored. In this study, the two main variants of the ubiquitous honey bee virus DWV as well as three major honey bee viruses (SBV, ABPV and BQCV) were analyzed from Varroa-destructor-parasitized pupae. More precisely, RT-qPCR was used to quantify and compare virus genome copies across honey bee pupae at the individual and subfamily levels (i.e., patrilines, sharing the same mother queen but with different drones as fathers). Additionally, virus genome copies were compared in cells parasitized by reproducing and non-reproducing mite foundresses to assess the role of this vector. Only DWV was detected in the samples, and the two variants of this virus significantly differed when comparing the sampling period, colonies and patrilines. Moreover, DWV-A and DWV-B exhibited different infection patterns, reflecting contrasting dynamics. Altogether, these results provide new insight into honey bee diseases and stress the need for more studies about the mechanisms of intra-colonial disease variation in social insects. Full article
(This article belongs to the Special Issue Microorganisms in Pollinators: Interactions with Other Factors)
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19 pages, 5210 KiB  
Article
Seed Meals from Brassica nigra and Eruca sativa Control Artificial Nosema ceranae Infections in Apis mellifera
by Antonio Nanetti, Luisa Ugolini, Giovanni Cilia, Eleonora Pagnotta, Lorena Malaguti, Ilaria Cardaio, Roberto Matteo and Luca Lazzeri
Microorganisms 2021, 9(5), 949; https://doi.org/10.3390/microorganisms9050949 - 28 Apr 2021
Cited by 31 | Viewed by 3556
Abstract
Nosema ceranae is a widespread parasite responsible for nosemosis Type C in Apis mellifera honey bees, reducing colony survival. The antibiotic fumagillin is the only commercial treatment available, but concerns are emerging about its persistence, safety, and pathogen resistance. The use of natural [...] Read more.
Nosema ceranae is a widespread parasite responsible for nosemosis Type C in Apis mellifera honey bees, reducing colony survival. The antibiotic fumagillin is the only commercial treatment available, but concerns are emerging about its persistence, safety, and pathogen resistance. The use of natural substances from Brassicaceae defatted seed meals (DSMs) with known antimicrobial and antioxidant properties was explored. Artificially infected bees were fed for 8 days with candies enriched with two concentrations, 2% and 4%, of two DSMs from Brassica nigra and Eruca sativa, containing a known amount of different glucosinolates (GSLs). The food palatability, GSL intake, bee survival, and treatment effects on N. ceranae spore counts were evaluated. Food consumption was higher for the two 2% DSM patties, for both B. nigra and E. sativa, but the GSL intake did not increase by increasing DSM to 4%, due to the resulting lower palatability. The 2% B. nigra patty decreased the bee mortality, while the higher concentration had a toxic effect. The N. ceranae control was significant for all formulates with respect to the untreated control (312,192.6 +/− 14,443.4 s.e.), and was higher for 4% B. nigra (120,366.3 +/− 13,307.1 s.e.). GSL hydrolysis products, the isothiocyanates, were detected and quantified in bee gut tissues. Brassicaceae DSMs showed promising results for their nutraceutical and protective effects on bees artificially infected with N. ceranae spores at the laboratory level. Trials in the field should confirm these results. Full article
(This article belongs to the Special Issue Microorganisms in Pollinators: Interactions with Other Factors)
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13 pages, 9696 KiB  
Article
The Gut Microbiota Can Provide Viral Tolerance in the Honey Bee
by Christopher Dosch, Anja Manigk, Tabea Streicher, Anja Tehel, Robert J. Paxton and Simon Tragust
Microorganisms 2021, 9(4), 871; https://doi.org/10.3390/microorganisms9040871 - 17 Apr 2021
Cited by 45 | Viewed by 6873
Abstract
Adult honey bees host a remarkably consistent gut microbial community that is thought to benefit host health and provide protection against parasites and pathogens. Currently, however, we lack experimental evidence for the causal role of the gut microbiota in protecting the Western honey [...] Read more.
Adult honey bees host a remarkably consistent gut microbial community that is thought to benefit host health and provide protection against parasites and pathogens. Currently, however, we lack experimental evidence for the causal role of the gut microbiota in protecting the Western honey bees (Apis mellifera) against their viral pathogens. Here we set out to fill this knowledge gap by investigating how the gut microbiota modulates the virulence of a major honey bee viral pathogen, deformed wing virus (DWV). We found that, upon oral virus exposure, honey bee survival was significantly increased in bees with an experimentally established normal gut microbiota compared to control bees with a perturbed (dysbiotic) gut microbiota. Interestingly, viral titers were similar in bees with normal gut microbiota and dysbiotic bees, pointing to higher viral tolerance in bees with normal gut microbiota. Taken together, our results provide evidence for a positive role of the gut microbiota for honey bee fitness upon viral infection. We hypothesize that environmental stressors altering honey bee gut microbiota composition, e.g., antibiotics in beekeeping or pesticides in modern agriculture, could interact synergistically with pathogens, leading to negative effects on honey bee health and the epidemiology and impact of their viruses. Full article
(This article belongs to the Special Issue Microorganisms in Pollinators: Interactions with Other Factors)
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15 pages, 2947 KiB  
Article
Impact of Chronic Exposure to Sublethal Doses of Glyphosate on Honey Bee Immunity, Gut Microbiota and Infection by Pathogens
by Loreley Castelli, Sofía Balbuena, Belén Branchiccela, Pablo Zunino, Joanito Liberti, Philipp Engel and Karina Antúnez
Microorganisms 2021, 9(4), 845; https://doi.org/10.3390/microorganisms9040845 - 15 Apr 2021
Cited by 42 | Viewed by 5848
Abstract
Glyphosate is the most used pesticide around the world. Although different studies have evidenced its negative effect on honey bees, including detrimental impacts on behavior, cognitive, sensory and developmental abilities, its use continues to grow. Recent studies have shown that it also alters [...] Read more.
Glyphosate is the most used pesticide around the world. Although different studies have evidenced its negative effect on honey bees, including detrimental impacts on behavior, cognitive, sensory and developmental abilities, its use continues to grow. Recent studies have shown that it also alters the composition of the honey bee gut microbiota. In this study we explored the impact of chronic exposure to sublethal doses of glyphosate on the honey bee gut microbiota and its effects on the immune response, infection by Nosema ceranae and Deformed wing virus (DWV) and honey bee survival. Glyphosate combined with N. ceranae infection altered the structure and composition of the honey bee gut microbiota, for example by decreasing the relative abundance of the core members Snodgrassella alvi and Lactobacillus apis. Glyphosate increased the expression of some immune genes, possibly representing a physiological response to mitigate its negative effects. However, this response was not sufficient to maintain honey bee health, as glyphosate promoted the replication of DWV and decreased the expression of vitellogenin, which were accompanied by a reduced life span. Infection by N. ceranae also alters honey bee immunity although no synergistic effect with glyphosate was observed. These results corroborate previous findings suggesting deleterious effects of widespread use of glyphosate on honey bee health, and they contribute to elucidate the physiological mechanisms underlying a global decline of pollination services. Full article
(This article belongs to the Special Issue Microorganisms in Pollinators: Interactions with Other Factors)
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17 pages, 2337 KiB  
Article
RNA Interference-Mediated Knockdown of Genes Encoding Spore Wall Proteins Confers Protection against Nosema ceranae Infection in the European Honey Bee, Apis mellifera
by Nan He, Yi Zhang, Xin Le Duan, Jiang Hong Li, Wei-Fone Huang, Jay D. Evans, Gloria DeGrandi-Hoffman, Yan Ping Chen and Shao Kang Huang
Microorganisms 2021, 9(3), 505; https://doi.org/10.3390/microorganisms9030505 - 27 Feb 2021
Cited by 16 | Viewed by 4426
Abstract
Nosema ceranae (Opisthosporidia: Microsporidia) is an emergent intracellular parasite of the European honey bee (Apis mellifera) and causes serious Nosema disease which has been associated with worldwide honey bee colony losses. The only registered treatment for Nosema disease is fumagillin-b, and [...] Read more.
Nosema ceranae (Opisthosporidia: Microsporidia) is an emergent intracellular parasite of the European honey bee (Apis mellifera) and causes serious Nosema disease which has been associated with worldwide honey bee colony losses. The only registered treatment for Nosema disease is fumagillin-b, and this has raised concerns about resistance and off-target effects. Fumagillin-B is banned from use in honey bee colonies in many countries, particularly in Europe. As a result, there is an urgent need for new and effective therapeutic options to treat Nosema disease in honey bees. An RNA interference (RNAi)-based approach can be a potent strategy for controlling diseases in honey bees. We explored the therapeutic potential of silencing the sequences of two N. ceranae encoded spore wall protein (SWP) genes by means of the RNAi-based methodology. Our study revealed that the oral ingestion of dsRNAs corresponding to SWP8 and SWP12 used separately or in combination could lead to a significant reduction in spore load, improve immunity, and extend the lifespan of N. ceranae-infected bees. The results from the work completed here enhance our understanding of honey bee host responses to microsporidia infection and highlight that RNAi-based therapeutics are a promising treatment for honey bee diseases. Full article
(This article belongs to the Special Issue Microorganisms in Pollinators: Interactions with Other Factors)
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18 pages, 1443 KiB  
Article
Artificial Diets Modulate Infection Rates by Nosema ceranae in Bumblebees
by Tamara Gómez-Moracho, Tristan Durand, Cristian Pasquaretta, Philipp Heeb and Mathieu Lihoreau
Microorganisms 2021, 9(1), 158; https://doi.org/10.3390/microorganisms9010158 - 12 Jan 2021
Cited by 14 | Viewed by 2835
Abstract
Parasites alter the physiology and behaviour of their hosts. In domestic honey bees, the microsporidia Nosema ceranae induces energetic stress that impairs the behaviour of foragers, potentially leading to colony collapse. Whether this parasite similarly affects wild pollinators is little understood because of [...] Read more.
Parasites alter the physiology and behaviour of their hosts. In domestic honey bees, the microsporidia Nosema ceranae induces energetic stress that impairs the behaviour of foragers, potentially leading to colony collapse. Whether this parasite similarly affects wild pollinators is little understood because of the low success rates of experimental infection protocols. Here, we present a new approach for infecting bumblebees (Bombus terrestris) with controlled amounts of N. ceranae by briefly exposing individual bumblebees to parasite spores before feeding them with artificial diets. We validated our protocol by testing the effect of two spore dosages and two diets varying in their protein to carbohydrate ratio on the prevalence of the parasite (proportion of PCR-positive bumblebees), the intensity of parasites (spore count in the gut and the faeces), and the survival of bumblebees. Overall, insects fed a low-protein, high-carbohydrate diet showed the highest parasite prevalence (up to 70%) but lived the longest, suggesting that immunity and survival are maximised at different protein to carbohydrate ratios. Spore dosage did not affect parasite infection rate and host survival. The identification of experimental conditions for successfully infecting bumblebees with N. ceranae in the lab will facilitate future investigations of the sub-lethal effects of this parasite on the behaviour and cognition of wild pollinators. Full article
(This article belongs to the Special Issue Microorganisms in Pollinators: Interactions with Other Factors)
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18 pages, 1481 KiB  
Article
The Effect of Migratory Beekeeping on the Infestation Rate of Parasites in Honey Bee (Apis mellifera) Colonies and on Their Genetic Variability
by Laura Jara, Carlos Ruiz, Raquel Martín-Hernández, Irene Muñoz, Mariano Higes, José Serrano and Pilar De la Rúa
Microorganisms 2021, 9(1), 22; https://doi.org/10.3390/microorganisms9010022 - 23 Dec 2020
Cited by 21 | Viewed by 3678
Abstract
Migratory beekeeping is a widely extended practice aimed at increasing the yield of products and pollination services of honey bee colonies. However, it represents a stress factor, as it facilitates the dissemination of diseases and may compromise the genetic identity of the colonies [...] Read more.
Migratory beekeeping is a widely extended practice aimed at increasing the yield of products and pollination services of honey bee colonies. However, it represents a stress factor, as it facilitates the dissemination of diseases and may compromise the genetic identity of the colonies involved. To analyze the extent of these effects, pathogens infestation rate and genetic composition were monitored in a field experiment comparing stationary and migratory colonies sharing the same environmental conditions but differing in management (stationary vs. migratory) and genetic background. We studied the pathogens infestation rate (Varroa destructor, Nosema spp., and Deformed Wing Virus (DWV)) at four different times: before migratory operation, two weeks later, at the end of the migratory period, and two weeks after the return of the migratory hives. An increased incidence of V. destructor and Nosema ceranae and a lower DWV viral load were found in migratory colonies. Temporary changes in genetic diversity were detected regardless of colony type, suggesting that stressors other than management affect the genetic diversity of the colonies. Our study demonstrates that migratory practices have variable effects on the health and genetic diversity of honey bee colonies, which should be taken into account for the development of sustainable beekeeping. Full article
(This article belongs to the Special Issue Microorganisms in Pollinators: Interactions with Other Factors)
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11 pages, 1350 KiB  
Article
Dynamics of the Honeybee (Apis mellifera) Gut Microbiota Throughout the Overwintering Period in Canada
by Naomie Bleau, Sidki Bouslama, Pierre Giovenazzo and Nicolas Derome
Microorganisms 2020, 8(8), 1146; https://doi.org/10.3390/microorganisms8081146 - 29 Jul 2020
Cited by 29 | Viewed by 4914
Abstract
Microbial symbionts inhabiting the honeybee gut (i.e., gut microbiota) are essential for food digestion, immunity, and gut protection of their host. The taxonomic composition of the gut microbiota is dynamic throughout the honeybee life cycle and the foraging season. However, it remains unclear [...] Read more.
Microbial symbionts inhabiting the honeybee gut (i.e., gut microbiota) are essential for food digestion, immunity, and gut protection of their host. The taxonomic composition of the gut microbiota is dynamic throughout the honeybee life cycle and the foraging season. However, it remains unclear how drastic changes occurring in winter, such as food shortage and cold weather, impact gut microbiota dynamics. The objective of this study was to characterize the gut microbiota of the honeybee during the overwintering period in a northern temperate climate in Canada. The microbiota of nine honeybee colonies was characterized by metataxonomy of 16S rDNA between September 2017 and June 2018. Overall, the results showed that microbiota taxonomic composition experienced major compositional shifts in fall and spring. From September to November, Enterobacteriaceae decreased, while Neisseriaceae increased. From April to June, Orbaceae increased, whereas Rhizobiaceae nearly disappeared. Bacterial diversity of the gut microbiota decreased drastically before and after overwintering, but it remained stable during winter. We conclude that the honeybee gut microbiota is likely to be impacted by the important meteorological and dietary changes that take place before and after the overwintering period. Laboratory trials are needed to determine how the observed variations affect the honeybee health. Full article
(This article belongs to the Special Issue Microorganisms in Pollinators: Interactions with Other Factors)
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16 pages, 756 KiB  
Article
Interaction of Varroa destructor and Sublethal Clothianidin Doses during the Larval Stage on Subsequent Adult Honey Bee (Apis mellifera L.) Health, Cellular Immunity, Deformed Wing Virus Levels and Differential Gene Expression
by Nuria Morfin, Paul H. Goodwin and Ernesto Guzman-Novoa
Microorganisms 2020, 8(6), 858; https://doi.org/10.3390/microorganisms8060858 - 6 Jun 2020
Cited by 13 | Viewed by 4152
Abstract
Honeybees (Apis mellifera L.) are exposed to many parasites, but little is known about interactions with abiotic stressors on their health, particularly when affected as larvae. Larvae were exposed singly and in combination to the parasitic mite Varroa destructor and three sublethal [...] Read more.
Honeybees (Apis mellifera L.) are exposed to many parasites, but little is known about interactions with abiotic stressors on their health, particularly when affected as larvae. Larvae were exposed singly and in combination to the parasitic mite Varroa destructor and three sublethal doses of the neonicotinoid insecticide clothianidin to evaluate their effects on survivorship, weight, haemocyte counts, deformed wing virus (DWV) levels and gene expression of the adult bees that subsequently developed. Clothianidin significantly reduced bee weight at the highest dose and was associated with an increase in haemocyte counts at the lowest dose, whereas V. destructor parasitism increased DWV levels, reduced bee emergence, lowered weight and reduced haemocyte counts. An interaction between the two stressors was observed for weight at emergence. Among the differentially expressed genes (DEGs), V. destructor infestation resulted in broader down-regulatory effects related to immunity that was often shared with the combined stressors, while clothianidin resulted in a broader up-regulatory effect more related to central metabolic pathways that was often shared with the combined stressors. Parasites and abiotic stressors can have complex interactions, including additive effects on reduced weight, number of up-regulated DEGs and biological pathways associated with metabolism. Full article
(This article belongs to the Special Issue Microorganisms in Pollinators: Interactions with Other Factors)
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