Interactions between cooccurring lactic acid bacteria in honey bee hives

Applied and Environmental Microbiology

Volumn 81, Issue 20, 2015, Pages 7261-7270

  Rokop, Z P ^a   Horton, M A ^a   Newton, I L G ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTICS; CARBOHYDRATES; COMPLEX NETWORKS; FOOD PRODUCTS; LACTIC ACID; MICROORGANISMS;

BACTERIAL SPECIES; CO-OCCURRENCE; COCULTURE; COMPLEX PLANTS; LACTIC ACID BACTERIA; MICROBIAL COMMUNITIES; MICROBIOME; OPERATIONAL TAXONOMIC UNITS;

BACTERIA;

ARRAY; BACTERIUM; BIOASSAY; BIOTECHNOLOGY; CARBOHYDRATE; CELLS AND CELL COMPONENTS; CLADISTICS; GLUCOSE; GROWTH RATE; HONEYBEE; INOCULATION; LIGNIN; METABOLISM; MICROBIAL COMMUNITY; ORGANIC ACID; TAXONOMY;

APIS MELLIFERA; APOIDEA; BACTERIA (MICROORGANISMS); LACTOBACILLACEAE;

ANIMAL; BACTERIUM; BEE; CLASSIFICATION; GENETICS; ISOLATION AND PURIFICATION; LACTOBACILLUS; LACTOCOCCUS LACTIS; MICROBIOLOGY; MOLECULAR GENETICS; URTICARIA;

ANIMALS; BACTERIA; BEES; LACTOBACILLUS; LACTOCOCCUS LACTIS; MOLECULAR SEQUENCE DATA; URTICARIA;

EID: 84943338589     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01259-15     Document Type: Article

References (46)

1. Newton ILG, Roeselers G. 2012. The effect of training set on the classification of honey bee gut microbiota using the naive Bayesian classifier. BMC Microbiol 12:221. http://dx.doi.org/10.1186/1471-2180-12-221.
2. Martinson VG, Danforth BN, Minckley RL, Rueppell O, Tingek S, Moran NA. 2011. A simple and distinctive microbiota associated with honey bees and bumble bees. Mol Ecol 20:619-628. http://dx.doi.org/10.1111/j.1365-294X.2010.04959.x.
3. Moran NA, Hansen AK, Powell E, Sabree ZL. 2012. Distinctive gut microbiota of honey bees assessed using deep sampling from individual worker bees. PLoS One 7:e36393. http://dx.doi.org/10.1371/journal.pone.0036393.
4. Martinson VG, Moy J, Moran NA. 2012. Establishment of characteristic gut bacteria during development of the honeybee worker. Appl Environ Microbiol 78:2830-2840. http://dx.doi.org/10.1128/AEM.07810-11.
5. Powell JE, Martinson VG, Urban-Mead K, Moran NA. 2014. Routes of acquisition of the gut microbiota of Apis mellifera. Appl Environ Microbiol 80:7378-7387. http://dx.doi.org/10.1128/AEM.01861-14.
6. Haydak MH. 1970. Honey bee nutrition. Annu Rev Entomol 15:143. http://dx.doi.org/10.1146/annurev.en.15.010170.001043.
7. Vasquez A, Forsgren E, Fries I, Paxton RJ, Flaberg E, Szekely L, Olofsson TC. 2012. Symbionts as major modulators of insect health: lactic acid bacteria and honeybees. PLoS One 7:e33188. http://dx.doi.org/10.1371/journal.pone.0033188.
8. Vasquez A, Olofsson TC. 2009. The lactic acid bacteria involved in the production of bee pollen and bee bread. J Apic Res 48:189-195. http://dx.doi.org/10.3896/IBRA.1.48.3.07.
9. Danzeisen JL, Calvert AJ, Noll SL, McComb B, Sherwood JS, Logue CM, Johnson TJ. 2013. Succession of the turkey gastrointestinal bacterial microbiome related to weight gain. PeerJ 1:e237. http://dx.doi.org/10.7717/peerj.237.
10. Gillilland MG, Erb-Downward JR, Bassis CM, Shen MC, Toews GB, Young VB, Huffnagle GB. 2012. Ecological succession of bacterial communities during conventionalization of germ-free mice. Appl Environ Microbiol 78:2359-2366. http://dx.doi.org/10.1128/AEM.05239-11.
11. Lu J, Idris U, Harmon B, Hofacre C, Maurer JJ, Lee MD. 2003. Diversity and succession of the intestinal bacterial community of the maturing broiler chicken. Appl Environ Microbiol 69:6816-6824. http://dx.doi.org/10.1128/AEM.69.11.6816-6824.2003.
12. Favier CF, de Vos WM, Akkermans ADL. 2003. Development of bacterial and bifidobacterial communities in feces of newborn babies. Anaerobe 9:219-229. http://dx.doi.org/10.1016/j.anaerobe.2003.07.001.
13. Jangid K, Whitman WB, Condron LM, Turner BL, Williams MA. 2013. Soil bacterial community succession during long-term ecosystem development. Mol Ecol 22:3415-3424. http://dx.doi.org/10.1111/mec.12325.
14. Schutte UME, Abdo Z, Bent SJ, Williams CJ, Schneider GM, Solheim B, Forney LJ. 2009. Bacterial succession in a glacier foreland of the High Arctic. ISME J 3:1258-1268. http://dx.doi.org/10.1038/ismej.2009.71.
15. Koenig JE, Spor A, Scalfone N, Fricker AD, Stombaugh J, Knight R, Angenent LT, Ley RE. 2011. Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci U S A 108:4578-4585. http://dx.doi.org/10.1073/pnas.1000081107.
16. Brucker RM, Bordenstein SR. 2012. The roles of host evolutionary relationships (genus: Nasonia) and development in structuring microbial communities. Evolution 66:349-362. http://dx.doi.org/10.1111/j.1558-5646.2011.01454.x.
17. Carrasco P, Pérez-Cobas AE, van de Pol C, Baixeras J, Moya A, Latorre A. 2014. Succession of the gut microbiota in the cockroach Blattella germanica. Int Microbiol 17:79-109.
18. Hakim RS, Baldwin K, Smagghe G. 2010. Regulation of midgut growth, development and metamorphosis. Annu Rev Entomol 55:593-608. http://dx.doi.org/10.1146/annurev-ento-112408-085450.
19. Grubbs KJ, Scott JJ, Budsberg KJ, Read H, Balser TC, Currie CR. 2015. Unique honey bee (Apis mellifera) hive component-based communities as detected by a hybrid of phospholipid fatty-acid and fatty-acid methyl ester analyses. PLoS One 10:e0121697. http://dx.doi.org/10.1371/journal.pone.0121697.
20. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R. 2012. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621-1624. http://dx.doi.org/10.1038/ismej.2012.8.
21. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537-7541. http://dx.doi.org/10.1128/AEM.01541-09.
22. Szalay-Beko M, Palotai R, Szappanos B, Kovacs IA, Papp B, Csermely P. 2012. ModuLand plug-in for Cytoscape: determination of hierarchical layers of overlapping network modules and community centrality. Bioinformatics 28:2202-2204. http://dx.doi.org/10.1093/bioinformatics/bts352.
23. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30: 2725-2729. http://dx.doi.org/10.1093/molbev/mst197.
24. Vojvodic S, Rehan SM, Anderson KE. 2013. Microbial gut diversity of Africanized and European honey bee larval instars. PLoS One 8:e72106. http://dx.doi.org/10.1371/journal.pone.0072106.
25. Forsgren E, Olofsson TC, Vasquez A, Fries I. 2010. Novel lactic acid bacteria inhibiting Paenibacillus larvae in honey bee larvae. Apidologie 41:99-108. http://dx.doi.org/10.1051/apido/2009065.
26. McFrederick QS, Wcislo WT, Hout MC, Mueller UG. 2014. Host species and developmental stage, but not host social structure, affects bacterial community structure in socially polymorphic bees. FEMS Microbiol Ecol 88:398-406. http://dx.doi.org/10.1111/1574-6941.12302.
27. McFrederick QS, Cannone JJ, Gutell RR, Kellner K, Plowes RM, Mueller UG. 2013. Specificity between lactobacilli and hymenopteran hosts is the exception rather than the rule. Appl Environ Microbiol 79: 1803-1812. http://dx.doi.org/10.1128/AEM.03681-12.
28. Vojvodic S, Rehan SM, Anderson KE. 2013. Microbial gut diversity of Africanized and European honey bee larval instars. PLoS One 8:e72106. http://dx.doi.org/10.1371/journal.pone.0072106.
29. Endo A, Irisawa T, Futagawa-Endo Y, Sonomoto K, Itoh K, Takano K, Okada S, Dicks LM. 2011. Fructobacillus tropaeoli sp. nov., a fructophilic lactic acid bacterium isolated from a flower. Int J Syst Evol Microbiol 61:898-902. http://dx.doi.org/10.1099/ijs.0.023838-0.
30. Anderson KE, Sheehan TH, Mott BM, Maes P, Snyder L, Schwan MR, Walton A, Jones BM, Corby-Harris V. 2013. Microbial ecology of the hive and pollination landscape: bacterial associates from floral nectar, the alimentary tract and stored food of honey bees (Apis mellifera). PLoS One 8:e83125. http://dx.doi.org/10.1371/journal.pone.0083125.
31. Koch H, Schmid-Hempel P. 2011. Bacterial communities in central European bumblebees: low diversity and high specificity. Microb Ecol 62: 121-133. http://dx.doi.org/10.1007/s00248-011-9854-3.
32. Lee FJ, Rusch DB, Stewart FJ, Mattila HR, Newton IL. 2015. Saccharide breakdown and fermentation by the honey bee gut microbiome. Environ Microbiol 17:796-815. http://dx.doi.org/10.1111/1462-2920.12526.
33. Engel P, Martinson VG, Moran NA. 2012. Functional diversity within the simple gut microbiota of the honey bee. Proc Natl Acad Sci U S A 109:11002-11007. http://dx.doi.org/10.1073/pnas.1202970109.
34. Lee FJ, DB; Stewart FJ; Mattila HR; Newton ILG. 2015. Saccharide breakdown and fermentation by the honey bee gut microbiome. Environ Microbiol 17:796-815. http://dx.doi.org/10.1111/1462-2920.12526.
35. Brooks J, Shaw G. 1968. Chemical structure of exine of pollen walls and a new function for carotenoids in nature. Nature 219:532-533.
36. Graven P, DeKoster CG, Boon JJ, Bouman F. 1996. Structure and macromolecular composition of the seed coat of the Musaceae. Ann Bot London 77:105-122. http://dx.doi.org/10.1006/anbo.1996.0013.
37. Liu ZH, Ger MJ. 1997. Changes of enzyme activity during pollen germination in maize, and possible evidence of lignin synthesis. Aust J Plant Physiol 24:329-335. http://dx.doi.org/10.1071/PP96015.
38. Weng JK, Mo HP, Chapple C. 2010. Over-expression of F5H in COMTdeficient Arabidopsis leads to enrichment of an unusual lignin and disruption of pollen wall formation. Plant J 64:898-911. http://dx.doi.org/10.1111/j.1365-313X.2010.04391.x.
39. Nieminen TT, Sade E, Endo A, Johansson P, Björkroth J. 2014. The family Leuconostocaceae, p 215-240. In Rosenberg E, Lory S, Stackebrandt E, Thompson F (ed), The prokaryotes: firmicutes and tenericutes. Springer, Berlin, Germany.
40. Engel P, James RR, Koga R, Kwong WK, McFrederick QS, Moran NA. 2013. Standard methods for research on Apis mellifera gut symbionts. J Apic Res 52(4). http://dx.doi.org/10.3896/IBRA.1.52.4.07.
41. Evans JD, Lopez DL. 2004. Bacterial probiotics induce an immune response in the honey bee (Hymenoptera: Apidae). J Econ Entomol 97:752-756. http://dx.doi.org/10.1093/jee/97.3.752.
42. Olofsson TC, Vasquez A. 2008. Detection and identification of a novel lactic acid bacterial flora within the honey stomach of the honeybee Apis mellifera. Curr Microbiol 57:356-363. http://dx.doi.org/10.1007/s00284-008-9202-0.
43. Mattila HR, Rios D, Walker-Sperling V, Roeselers G, Newton I. 2012. Characterization of the active microbiotas associated with honey bees reveals healthier and broader communities when colonies are genetically diverse. PLoS One 7:e32962. http://dx.doi.org/10.1371/journal.pone.0032962.
44. Corby-Harris V, Snyder LA, Schwan MR, Maes P, McFrederick QS, Anderson KE. 2014. Origin and effect of Acetobacteraceae Alpha 2.2 in honey bee larvae and description of Parasaccharibacter apium gen. nov., sp. nov. Appl Environ Microbiol 80:7460-7472. http://dx.doi.org/10.1128/AEM.02043-14.
45. Tarpy DR, Mattila HR, Newton ILG. 2015. Development of the honey bee gut microbiome throughout the queen-rearing process. Appl Environ Microbiol 81:3182-3191. http://dx.doi.org/10.1128/AEM.00307-15.
46. Evans JD. 2003. Diverse origins of tetracycline resistance in the honey bee bacterial pathogen Paenibacillus larvae. J Invertebr Pathol 83:46-50. http://dx.doi.org/10.1016/S0022-2011(03)00039-9.