Literature DB >> 27482088

Early gut colonizers shape parasite susceptibility and microbiota composition in honey bee workers.

Ryan S Schwarz1, Nancy A Moran2, Jay D Evans3.   

Abstract

Microbial symbionts living within animal guts are largely composed of resident bacterial species, forming communities that often provide benefits to the host. Gut microbiomes of adult honey bees (Apis mellifera) include core residents such as the betaproteobacterium Snodgrassella alvi, alongside transient parasites such as the protozoan Lotmaria passim To test how these species affect microbiome composition and host physiology, we administered S alvi and/or L passim inocula to newly emerged worker bees from four genetic backgrounds (GH) and reared them in normal (within hives) or stressed (protein-deficient, asocial) conditions. Microbiota acquired by normal bees were abundant but quantitatively differed across treatments, indicating treatment-associated dysbiosis. Pretreatment with S. alvi made normal bees more susceptible to L. passim and altered developmental and detoxification gene expression. Stressed bees were more susceptible to L. passim and were depauperate in core microbiota, yet supplementation with S. alvi did not alter this susceptibility. Microbiomes were generally more variable by GH in stressed bees, which also showed opposing and comparatively reduced modulation of gene expression responses to treatments compared with normal bees. These data provide experimental support for a link between altered gut microbiota and increased parasite and pathogen prevalence, as observed from honey bee colony collapse disorder.

Entities:  

Keywords:  cytochrome P450; dysbiosis; microbial interaction; parasitism; vitellogenin

Mesh:

Substances:

Year:  2016        PMID: 27482088      PMCID: PMC4995961          DOI: 10.1073/pnas.1606631113

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  69 in total

1.  Genetic diversity, parasite prevalence and immunity in wild bumblebees.

Authors:  Penelope R Whitehorn; Matthew C Tinsley; Mark J F Brown; Ben Darvill; Dave Goulson
Journal:  Proc Biol Sci       Date:  2010-10-06       Impact factor: 5.349

2.  Bumble-bee foragers infected by a gut parasite have an impaired ability to utilize floral information.

Authors:  Robert J Gegear; Michael C Otterstatter; James D Thomson
Journal:  Proc Biol Sci       Date:  2006-05-07       Impact factor: 5.349

3.  Variation in gut microbial communities and its association with pathogen infection in wild bumble bees (Bombus).

Authors:  Daniel P Cariveau; J Elijah Powell; Hauke Koch; Rachael Winfree; Nancy A Moran
Journal:  ISME J       Date:  2014-04-24       Impact factor: 10.302

Review 4.  Multiorganismal insects: diversity and function of resident microorganisms.

Authors:  Angela E Douglas
Journal:  Annu Rev Entomol       Date:  2014-10-08       Impact factor: 19.686

5.  Genomics of the honey bee microbiome.

Authors:  Nancy A Moran
Journal:  Curr Opin Insect Sci       Date:  2015-08-01       Impact factor: 5.186

6.  Population genomics of the honey bee reveals strong signatures of positive selection on worker traits.

Authors:  Brock A Harpur; Clement F Kent; Daria Molodtsova; Jonathan M D Lebon; Abdulaziz S Alqarni; Ayman A Owayss; Amro Zayed
Journal:  Proc Natl Acad Sci U S A       Date:  2014-01-31       Impact factor: 11.205

7.  Social immunity in honeybees (Apis mellifera): transcriptome analysis of varroa-hygienic behaviour.

Authors:  Y Le Conte; C Alaux; J-F Martin; J R Harbo; J W Harris; C Dantec; D Séverac; S Cros-Arteil; M Navajas
Journal:  Insect Mol Biol       Date:  2011-03-24       Impact factor: 3.585

8.  Characterization of Drosophila melanogaster cytochrome P450 genes.

Authors:  Henry Chung; Tamar Sztal; Shivani Pasricha; Mohan Sridhar; Philip Batterham; Phillip J Daborn
Journal:  Proc Natl Acad Sci U S A       Date:  2009-03-16       Impact factor: 11.205

9.  Molecular detection of protozoan parasites infecting Apis mellifera colonies in Japan.

Authors:  Tomomi Morimoto; Yuriko Kojima; Mikio Yoshiyama; Kiyoshi Kimura; Bu Yang; Guangda Peng; Tatsuhiko Kadowaki
Journal:  Environ Microbiol Rep       Date:  2012-09-07       Impact factor: 3.541

10.  Predictive markers of honey bee colony collapse.

Authors:  Benjamin Dainat; Jay D Evans; Yan Ping Chen; Laurent Gauthier; Peter Neumann
Journal:  PLoS One       Date:  2012-02-23       Impact factor: 3.240

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  62 in total

1.  Metabolism of Fructophilic Lactic Acid Bacteria Isolated from the Apis mellifera L. Bee Gut: Phenolic Acids as External Electron Acceptors.

Authors:  Pasquale Filannino; Raffaella Di Cagno; Rocco Addante; Erica Pontonio; Marco Gobbetti
Journal:  Appl Environ Microbiol       Date:  2016-09-16       Impact factor: 4.792

2.  Changes in the Bacteriome of Honey Bees Associated with the Parasite Varroa destructor, and Pathogens Nosema and Lotmaria passim.

Authors:  Jan Hubert; Martina Bicianova; Ondrej Ledvinka; Martin Kamler; Philip J Lester; Marta Nesvorna; Jan Kopecky; Tomas Erban
Journal:  Microb Ecol       Date:  2016-10-11       Impact factor: 4.552

3.  Cadmium and Selenate Exposure Affects the Honey Bee Microbiome and Metabolome, and Bee-Associated Bacteria Show Potential for Bioaccumulation.

Authors:  Jason A Rothman; Laura Leger; Jay S Kirkwood; Quinn S McFrederick
Journal:  Appl Environ Microbiol       Date:  2019-10-16       Impact factor: 4.792

4.  Temperature dependence of parasitic infection and gut bacterial communities in bumble bees.

Authors:  Evan C Palmer-Young; Lyna Ngor; Rodrigo Burciaga Nevarez; Jason A Rothman; Thomas R Raffel; Quinn S McFrederick
Journal:  Environ Microbiol       Date:  2019-11-04       Impact factor: 5.491

5.  Gut and Whole-Body Microbiota of the Honey Bee Separate Thriving and Non-thriving Hives.

Authors:  Céline Ribière; Claire Hegarty; Hannah Stephenson; Padraig Whelan; Paul W O'Toole
Journal:  Microb Ecol       Date:  2018-11-22       Impact factor: 4.552

6.  Triplex real-time PCR for detection of Crithidia mellificae and Lotmaria passim in honey bees.

Authors:  Guang Xu; Evan Palmer-Young; Kim Skyrm; Timothy Daly; Martha Sylvia; Anne Averill; Stephen Rich
Journal:  Parasitol Res       Date:  2017-12-27       Impact factor: 2.289

7.  Longitudinal Effects of Supplemental Forage on the Honey Bee (Apis mellifera) Microbiota and Inter- and Intra-Colony Variability.

Authors:  Jason A Rothman; Mark J Carroll; William G Meikle; Kirk E Anderson; Quinn S McFrederick
Journal:  Microb Ecol       Date:  2018-02-03       Impact factor: 4.552

Review 8.  Honey bees as models for gut microbiota research.

Authors:  Hao Zheng; Margaret I Steele; Sean P Leonard; Erick V S Motta; Nancy A Moran
Journal:  Lab Anim (NY)       Date:  2018-10-23       Impact factor: 12.625

9.  Into the wild: microbiome transplant studies need broader ecological reality.

Authors:  Christopher J Greyson-Gaito; Timothy J Bartley; Karl Cottenie; Will M C Jarvis; Amy E M Newman; Mason R Stothart
Journal:  Proc Biol Sci       Date:  2020-02-26       Impact factor: 5.349

10.  Microbiome Structure Influences Infection by the Parasite Crithidia bombi in Bumble Bees.

Authors:  Blair K Mockler; Waldan K Kwong; Nancy A Moran; Hauke Koch
Journal:  Appl Environ Microbiol       Date:  2018-03-19       Impact factor: 4.792

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