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Honeybee-specific lactic acid bacterial supplements have no effect on American foulbrood infected honeybee colonies

Stephan, Jörg G; Lamei, Sepideh LU ; Pettis, Jeffery S; Riesbeck, Kristian LU ; de Miranda, Joachim R and Forsgren, Eva (2019) In Applied and Environmental Microbiology 85(13).
Abstract

Paenibacillus larvae, causative agent of American Foulbrood (AFB), is the primary bacterial pathogen affecting honeybees and beekeeping. The main methods for controlling AFB are incineration of diseased colonies or prophylactic antibiotic treatment (e.g. tylosin), neither of which is fully satisfactory. The search for superior means for controlling AFB has led to an increased interest in the natural relationships between the honeybee pathogenic and mutualistic microorganisms, and in particular the antagonistic effects of honeybee-specific Lactic Acid Bacteria (hbs-LAB) against P. larvae These effects have only been demonstrated on individual larvae in controlled laboratory bioassays. Here we investigated whether supplemental... (More)

Paenibacillus larvae, causative agent of American Foulbrood (AFB), is the primary bacterial pathogen affecting honeybees and beekeeping. The main methods for controlling AFB are incineration of diseased colonies or prophylactic antibiotic treatment (e.g. tylosin), neither of which is fully satisfactory. The search for superior means for controlling AFB has led to an increased interest in the natural relationships between the honeybee pathogenic and mutualistic microorganisms, and in particular the antagonistic effects of honeybee-specific Lactic Acid Bacteria (hbs-LAB) against P. larvae These effects have only been demonstrated on individual larvae in controlled laboratory bioassays. Here we investigated whether supplemental administration of hbs-LAB had a similar beneficial effect on P. larvae infection at colony level. We compared experimentally AFB-infected colonies treated with hbs-LAB supplements to untreated and tylosin-treated colonies, recorded AFB symptoms, bacterial spore levels and two measures of colony health. To account for the complexity of a bee colony we focused on (Bayesian) probabilities and magnitudes of effect sizes. Tylosin reduced AFB disease symptoms but also had a negative effect on colony strength. The tylosin treatment did not, however, affect P. larvae spore levels, and might therefore "mask" the potential for disease. Hbs-LAB tended to reduce brood size in the short-term, but was unlikely to affect AFB symptoms or spores. These results do not contradict demonstrated antagonistic effects of hbs-LAB against P. larvae at the individual bee level, but rather suggest that supplementary administration of hbs-LAB may not be the most effective way to harness these beneficial effects at colony level.ImportanceThe previously demonstrated antagonistic effects of honeybee-derived bacterial microbiota on the infectivity and pathogenicity of P. larvae in laboratory bioassays has identified a possible new approach to AFB control. However, honeybee colonies are complex super-organisms where social immune defenses play a major role in resistance against disease at the colony-level. Few studies have investigated the effect of beneficial microorganisms on bee diseases at the colony level. Effects observed at the individual bee level do not necessarily translate into similar effects at the colony level. This study partially fills this gap by showing that, unlike at individual level, hbs-LAB supplements did not affect AFB symptoms at colony level. The inference is that the mechanisms regulating the honeybee microbial dynamics within a colony are too strong to manipulate positively through supplemental feeding of live hbs-LAB, and that new potential remedies identified through laboratory research have to be tested thoroughly in situ, in colonies.

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published
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Applied and Environmental Microbiology
volume
85
issue
13
publisher
American Society for Microbiology
external identifiers
  • scopus:85068065580
ISSN
0099-2240
DOI
10.1128/AEM.00606-19
language
English
LU publication?
yes
id
18177f15-52f2-4e08-92c8-fc9c6a35db5a
date added to LUP
2019-06-07 15:39:27
date last changed
2019-11-13 05:35:34
@article{18177f15-52f2-4e08-92c8-fc9c6a35db5a,
  abstract     = {<p>Paenibacillus larvae, causative agent of American Foulbrood (AFB), is the primary bacterial pathogen affecting honeybees and beekeeping. The main methods for controlling AFB are incineration of diseased colonies or prophylactic antibiotic treatment (e.g. tylosin), neither of which is fully satisfactory. The search for superior means for controlling AFB has led to an increased interest in the natural relationships between the honeybee pathogenic and mutualistic microorganisms, and in particular the antagonistic effects of honeybee-specific Lactic Acid Bacteria (hbs-LAB) against P. larvae These effects have only been demonstrated on individual larvae in controlled laboratory bioassays. Here we investigated whether supplemental administration of hbs-LAB had a similar beneficial effect on P. larvae infection at colony level. We compared experimentally AFB-infected colonies treated with hbs-LAB supplements to untreated and tylosin-treated colonies, recorded AFB symptoms, bacterial spore levels and two measures of colony health. To account for the complexity of a bee colony we focused on (Bayesian) probabilities and magnitudes of effect sizes. Tylosin reduced AFB disease symptoms but also had a negative effect on colony strength. The tylosin treatment did not, however, affect P. larvae spore levels, and might therefore "mask" the potential for disease. Hbs-LAB tended to reduce brood size in the short-term, but was unlikely to affect AFB symptoms or spores. These results do not contradict demonstrated antagonistic effects of hbs-LAB against P. larvae at the individual bee level, but rather suggest that supplementary administration of hbs-LAB may not be the most effective way to harness these beneficial effects at colony level.ImportanceThe previously demonstrated antagonistic effects of honeybee-derived bacterial microbiota on the infectivity and pathogenicity of P. larvae in laboratory bioassays has identified a possible new approach to AFB control. However, honeybee colonies are complex super-organisms where social immune defenses play a major role in resistance against disease at the colony-level. Few studies have investigated the effect of beneficial microorganisms on bee diseases at the colony level. Effects observed at the individual bee level do not necessarily translate into similar effects at the colony level. This study partially fills this gap by showing that, unlike at individual level, hbs-LAB supplements did not affect AFB symptoms at colony level. The inference is that the mechanisms regulating the honeybee microbial dynamics within a colony are too strong to manipulate positively through supplemental feeding of live hbs-LAB, and that new potential remedies identified through laboratory research have to be tested thoroughly in situ, in colonies.</p>},
  articleno    = {e00606-19},
  author       = {Stephan, Jörg G and Lamei, Sepideh and Pettis, Jeffery S and Riesbeck, Kristian and de Miranda, Joachim R and Forsgren, Eva},
  issn         = {0099-2240},
  language     = {eng},
  month        = {04},
  number       = {13},
  publisher    = {American Society for Microbiology},
  series       = {Applied and Environmental Microbiology},
  title        = {Honeybee-specific lactic acid bacterial supplements have no effect on American foulbrood infected honeybee colonies},
  url          = {http://dx.doi.org/10.1128/AEM.00606-19},
  volume       = {85},
  year         = {2019},
}