Social immunity in honey bees: royal jelly as a vehicle in transferring bacterial pathogen fragments between nestmates

Harwood, Gyan; Salmela, Heli; Freitak, Dalial; Amdam, Gro V.

doi:10.1242/jeb.231076

Cited by 26 publications

(30 citation statements)

References 78 publications

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“…Thus, this review shows how understanding the mechanisms by which invertebrates manage their environmental adaptability can provide insights into how humans protect themselves against their own pathogens. Honey bees are another example of this idea, in which individuals are protected against micro pathogens via the concept of social immunity [50].…”

Section: Discussionmentioning

confidence: 99%

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Oxygen and Redox Reactions Contribute to the Protection of Free-Living and Parasite Helminths against Pathogens and/or Host Response

Plancarte¹,

Nava²

2022

Parasitic Helminths and Zoonoses - From Basic to Applied Research

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Millions of years ago, the reductive atmosphere environment of Earth was replaced by an oxidative one because of redox reactions. These conditions allowed aerobic organisms to populate the planet and control the toxicity of oxygen. Aerobic organisms began to produce reactive oxygen species (ROS) via oxygen redox reactions and used them for their physiology process. Free-living helminths appeared in the early Paleozoic era and parasite helminths in the late same era. Free-living helminths, such as Caenorhabditis elegans and earthworms, have been used as host models to understand their micro pathogen defenses, particularly those associated with ROS. We speculate that the micro pathogens of C. elegans are equivalent to the parasite helminth hosts in terms of generating a worm’s defense response. Therefore, parasite helminths may share similar defense mechanisms to humans, as in C. elegans. This last observation suggests the existence of a conservative pathogen protection process for centuries. This review discusses the evolution of oxygen molecules and redox reactions, as well as of the Earth’s atmosphere, and changes over time in the protection of helminths mechanisms. These mechanisms have been so successful that have improved our understanding and have had a positive impact on humans.

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Section: Discussionmentioning

confidence: 99%

“…50 , is a parameter giving the inhibitory concentration causing 50% inhibition; Ki is the inhibition catalytic constant value; %F, is the % of Ts26GST intrinsic fluorescence quenching; ND, not determined. (Exp.Par.…”

mentioning

confidence: 99%

Oxygen and Redox Reactions Contribute to the Protection of Free-Living and Parasite Helminths against Pathogens and/or Host Response

Plancarte¹,

Nava²

2022

Parasitic Helminths and Zoonoses - From Basic to Applied Research

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“…We note that host niches and associated microbiotas are far more complex than discussed, and that the con rmation of a core colony microbiota will require further iteration and experimentation. Given the variety of social behaviors and microbes throughout the social environment [122], the behavioral and physiological processes associated with microbial odors or microbe-associated molecular patterns is an open question [68]. Hygienic worker behavior is presently de ned by response to death-associated larval odors, and removal behavior by adult workers [123,124].…”

Section: Conclusion/perspectivementioning

confidence: 99%

“…The gland can also react more proximally to colony-level challenge associated with a variety of social processes like emergency queen rearing [66,67]. In addition to providing shared nutrition, jelly may transmit immune training molecular patterns across generations, extend life expectancy, modulate microbiota structure and prevent opportunistic disease [67][68][69]. Gene expression associated with individual and social immunity is costly, and only generated by well-nourished individuals [61,70].…”

Section: Introductionmentioning

confidence: 99%

Gut and Colony Microbiota of Honey Bees Apis mellifera: Social Immunity, Opportunistic Disease and Survival Overwinter.

Anderson¹,

Maes

2021

Preprint

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BackgroundOverwintering is a major contributor to honey bee colony loss and involves changes in environmental conditions, host physiology and group behavior that influence disease susceptibility. Honey bees possess a secretory head gland that interfaces with the extended colony environment on many levels, producing pro-oxidants, antioxidants and antimicrobial peptides. With the coming of winter, colonies produce a long-lived (diutinus) worker phenotype that survives until environmental conditions improve. We used a known-age worker cohort to investigate microbiome integrity and social gene expression of diutinus workers overwinter. We provide additional context by contrasting host-microbial interactions from warm outdoor and cold indoor overwintering environments. ResultsWe produce the first evidence that social immune gene expression is associated with the core hindgut and colony microbiota in honey bees, and highlight the midgut as a target of opportunistic disease overwinter. We discovered a distinct physiological and microbiological trajectory for diutinus workers that differs drastically from younger, short-lived workers in the colony. Diutinus bees were associated with decreased fungal load and decreased bacterial diversity, and increased core microbiota and longevity. Colonies overwintered indoors maintained a stable or improved microbiota structure and complimentary gene expression overwinter. In contrast, workers from colonies overwintered outdoors in warm southern conditions possessed changes co-occurring throughout the alimentary tract microbiota that suggest opportunistic disease progression and resistance in diutinus workers, but susceptibility to opportunistic disease in younger workers that emerged during the winter, including increases in Enterobacteriaceae, fungal load and bacterial diversity abundance. ConclusionsOur results highlight social selection pressures that shaped the colony and hindgut microbiome with evolution to a perennial life history. The results are consistent with a “group level” explanation of social immunity, including host associations with the colony microbiota, and a social immune response by long-lived diutinus workers to accompany microbial opportunism. The cost/benefit ratio associated with limited expression of the diutinus phenotype may be a strong determinant of colony survival overwinter. The relationship of colony and gut microbiota with social immune function highlights the range of host-microbial interaction associated with the honey bee superorganism, and its potential influence on colony health, disease resistance and gut integrity.

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“…The gland can also react more proximally to colony-level challenge associated with a variety of social processes like emergency queen rearing 43,44 . In addition to providing shared nutrition, jelly produced in the HPG may transmit immune training molecular patterns across generations, extend life expectancy, modulate microbiota structure and prevent opportunistic disease [44][45][46] . Gene expression associated with individual and social immunity is costly, and only generated by well-nourished individuals 38,47 .…”

Section: Introductionmentioning

confidence: 99%

Gut and Colony Microbiota of Honey Bees: Social Immunity and Opportunism Overwinter

Anderson¹,

Maes²

2021

Preprint

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Overwintering is a major contributor to honey bee colony loss and involves factors that influence disease susceptibility. Honey bees possess a secretory head gland that interfaces with the extended social environment on many levels. With the coming of winter, colonies produce a long-lived (diutinus) worker phenotype that survives until environmental conditions improve. We used a known-age worker cohort to investigate microbiome integrity and social gene expression of diutinus workers overwinter. We provide additional context by contrasting host-microbial interactions from warm outdoor and cold indoor overwintering environments. Our results provide the first evidence that social immune gene expression is associated with diutinus bees, and highlight the midgut as a target of opportunistic disease overwinter. Host microbial interactions suggest opportunistic disease progression and resistance in diutinus workers, but susceptibility to opportunistic disease in younger workers that emerged during the winter, including increases in Enterobacteriaceae, fungal load and bacterial diversity abundance. The results are consistent with increased social immunity overwinter, including host associations with the colony microbiota, and a social immune response by long-lived diutinus workers to combat microbial opportunism. The cost/benefit ratio associated with limited expression of the diutinus phenotype may be a strong determinant of colony survival overwinter.

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Social immunity in honey bees: royal jelly as a vehicle in transferring bacterial pathogen fragments between nestmates

Cited by 26 publications

References 78 publications

Oxygen and Redox Reactions Contribute to the Protection of Free-Living and Parasite Helminths against Pathogens and/or Host Response

Oxygen and Redox Reactions Contribute to the Protection of Free-Living and Parasite Helminths against Pathogens and/or Host Response

Gut and Colony Microbiota of Honey Bees Apis mellifera: Social Immunity, Opportunistic Disease and Survival Overwinter.

Gut and Colony Microbiota of Honey Bees: Social Immunity and Opportunism Overwinter

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