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From Microhabitat of Floral Nectar Up to Biogeographic Scale: Novel Insights on Neutral and Niche Bacterial Assemblies

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Abstract

Microbial model systems are very useful in addressing macro-ecological questions. Two major theories exist to date, to explain the community structure of organisms: (1) the dispersal (neutral) assembly theory which predicts that community similarity decreases with increasing geographic distance, independent of any environmental variables, and (2) the niche assembly theory which predicts that the communities’ compositions are more homogeneous among sites characterized by similar environmental conditions. Our study system offered a unique opportunity to investigate the relative role of environmental conditions and spatial factors in shaping community composition. We explored the bacterial community composition (BCC) of Nicotiana glauca floral nectar using the Illumina MiSeq technique at three spatial scales (plants, site, and region) and two taxonomic levels. Floral nectar samples were collected from 69 N. glauca plants at 11 different sites along a 200-km transect in Israel, along three biogeographic regions. A distance decay of BCC was found among all plants throughout Israel, but such pattern was not found among either sites or biogeographical regions. The BCC was also governed by environmental conditions in all examined scales (from the plant up to the biogeographical region). We also found that taxonomic resolution (89 and 97% sequence identity for clustering operational taxonomic units) affected the results of these BCC analyses. Hence, our study revealed that the BCC in N. glauca floral nectar is shaped by both the environmental conditions and the distance between plants, depending on the sampling scale under examination as well as by taxonomic resolution.

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References

  1. Lomolino MV, Riddle BR, Whittaker R, Brown JH (2010) Biogeography. 4th Edn. Sinauer Associates

  2. Foissner W (2006) Biogeography and dispersal of micro-organisms: a review emphasizing protists. Acta Protozool. 45:111–136

    Google Scholar 

  3. Green J, Bohannan BJM (2006) Spatial scaling of microbial biodiversity. Trends Ecol. Evol. 21:501–507

    Article  PubMed  Google Scholar 

  4. Ramette A, Tiedje JM (2007) Biogeography: an emerging cornerstone for understanding prokaryotic diversity, ecology, and evolution. Microb. Ecol. 53:197–207

    Article  PubMed  Google Scholar 

  5. Lindström ES, Langenheder S (2012) Local and regional factors influencing bacterial community assembly. Environ. Microbiol. Rep. 4:1–9

    Article  PubMed  Google Scholar 

  6. Martiny JBH, Bohannan BJ, Brown JH, Colwell RK, Fuhrman JA, Green JL, et al. (2006) Microbial biogeography: putting microorganisms on the map. Nature Rev Microbiol 4:102–112

    Article  CAS  Google Scholar 

  7. Hanson CA, Fuhrman JA, Horner-Devine MC, Martiny JB (2012) Beyond biogeographic patterns: processes shaping the microbial landscape. Nature Rev Microbiol 10:497–506

    CAS  Google Scholar 

  8. Jessup CM, Kassen R, Forde SE, Kerr B, Buckling A, Rainey PB, et al. (2004) Big questions, small worlds: microbial model systems in ecology. Trends Ecol. Evol. 19:189–197

    Article  PubMed  Google Scholar 

  9. Baas-Becking LGM (1934) Geobiologie of inleiding tot de milieukunde. W P Van Stockum, Zoon

  10. MacArthur RH (1967) The theory of island biogeography. Princeton University Press

  11. Hubbell SP (2001) The unified neutral theory of species abundance and diversity. Princeton University Press, Princeton, NJ

    Google Scholar 

  12. Chesson P (2000) Mechanisms of maintenance of species diversity. Annu. Rev. Ecol. Evol. Syst. 31:343–366

    Article  Google Scholar 

  13. Levine JM, HilleRisLambers J (2009) The importance of niches for the maintenance of species diversity. Nature 461:254–257

    Article  CAS  PubMed  Google Scholar 

  14. Leibold MA, Holyoak M, Mouquet N, Amarasekare P, Chase JM, Hoopes MF, et al. (2004) The metacommunity concept: a framework for multi-scale community ecology. Ecol. Lett. 7:601–613

    Article  Google Scholar 

  15. Tilman D (2004) Niche tradeoffs, neutrality, and community structure: a stochastic theory of resource competition, invasion, and community assembly. PNAS 101:10854–10861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Tindall BJ, Rosselló-Móra R, Busse HJ, Ludwig W, Kämpfer P (2010) Notes on the characterization of prokaryote strains for taxonomic purposes. Int. J. Syst. Evol. Microbiol. 60:249–266

    Article  CAS  PubMed  Google Scholar 

  17. Hamady M, Knight R (2009) Microbial community profiling for human microbiome projects: tools, techniques, and challenges. Genome Res. 19:1141–1152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Chainho P, Costa JL, Chaves ML, Dauer DM, Costa MJ (2007) Influence of seasonal variability in benthic invertebrate community structure on the use of biotic indices to assess the ecological status of a Portuguese estuary. Mar. Pollut. Bull. 54:1586–1597

    Article  CAS  PubMed  Google Scholar 

  19. Bacci T, Trabucco B, Marzialetti S, Marusso V, Lomiri S, Vani D, et al. (2009) Taxonomic sufficiency in two case studies: where does it work better? Mar. Ecol. 30:13–19

    Article  Google Scholar 

  20. Reiss J, Brindle JR, Montoya JM, Woodward G (2009) Emerging horizons in biodiversity and ecosystem functioning research. Trends Ecol. Evol. 24:505–514

    Article  PubMed  Google Scholar 

  21. Cavanaugh KC, Stephen-Gosnell J, Davis SL, Ahumada J, Boundja P, Clarck DB, et al. (2014) Carbon storage in tropical forests correlates with taxonomic diversity and functional dominance on a global scale. Global Ecol Bio- geogr. doi:10.1111/geb.12143

    Google Scholar 

  22. Forcone A, Galetto L, Bernardello L (1997) Floral nectar chemical composition of some species from Patagonia. Biochem. Syst. Ecol. 25:395–340

    Article  CAS  Google Scholar 

  23. Fridman S, Izhaki I, Gerchman Y, Halpern M (2012) Bacterial communities in floral nectar. Environ Microbiol Report 4:97–104

    Article  Google Scholar 

  24. Alvarez-Perez S, Herrera CM (2013) Composition richness and non-random assembly of culturable bacterial-microfungal communities in floral nectar of Mediterranean plants. FEMS Microbiol. Ecol. 83:685–699

    Article  CAS  PubMed  Google Scholar 

  25. Alvarez-Perez S, Herrera CM, de Vega C (2012) Zooming-in on floral nectar: a first exploration of nectar-associated bacteria in wild plant communities. FEMS Microbiol. Ecol. 80:591–602

    Article  CAS  PubMed  Google Scholar 

  26. Aizenberg-Gershtein Y, Izhaki I, Halpern M (2013) Do honeybees shape the bacterial community composition in floral nectar? PLoS One 8:e67556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Junker RR, Keller A (2015) Microhabitat heterogeneity across leaves and flower organs promotes bacterial diversity. FEMS Microbiol. Ecol. 91:1–7

    Article  Google Scholar 

  28. Samuni-Blank M, Izhaki I, Laviad S, Bar-Massada A, Gerchman Y, Halpern M (2014) The role of abiotic environmental conditions, geographical distance and herbivory in shaping bacterial community composition in floral nectar. PLoS One 9:e99107

    Article  PubMed  PubMed Central  Google Scholar 

  29. Aleklett K, Hart M, Shade A (2014) The microbial ecology of flowers: an emerging frontier in phyllosphere research. Botany 92:253–266

    Article  Google Scholar 

  30. Peck RL (2015) Nectar: production, chemical composition and benefits to animals and plants. Nova Science Pub Inc

  31. Herrera CM, Pozo MI, Medrano M (2013) Yeasts in nectar of an early-blooming herb: sought by bumble bees, detrimental to plant fecundity. Ecology 94:273–279

    Article  PubMed  Google Scholar 

  32. Vannette RL, Gauthier ML, Fukami T (2013) Nectar bacteria, but not yeast, weaken a plant—pollinator mutualism. Proc. Biol. Sci. 280:20122601

    Article  PubMed  PubMed Central  Google Scholar 

  33. Ollerton J, Watts S, Connerty S, Lock J, Parker L, Wilson I, et al. (2012) Pollination ecology of the invasive tree tobacco Nicotiana glauca: comparisons across native and non-native ranges. J Pollinat Ecol 9:85–95

    Google Scholar 

  34. Bornmuller J (1898) Ein beitrag zur kenntnis der flora von Syrien und Palastina. Verhandlungen der Zoologisch-Botanischen Gesellschaft in Wien 48:544–653

    Google Scholar 

  35. Hernandez HM (1981) Sobre la ecologia reproductiva de Nicotiana glauca Grah: Unamaleza de distribucion cosmopolita. Bol Soc Bot México 41:47–73

    Google Scholar 

  36. Tadmor-Melamed H, Markman S, Arieli A, Distl M, Wink M, Izhaki I (2004) Limited ability of Palestine sunbirds Nectarinia osea to cope with pyridine alkaloids in nectar of tree tobacco Nicotiana glauca. Funct. Ecol. 18:844–850

    Article  Google Scholar 

  37. Moonsamy PV, Williams T, Bonella P, Holcomb CL, Höglund BN, Hillman G, et al. (2013) High throughput HLA genotyping using 454 sequencing and the Fluidigm Access Array™ system for simplified amplicon library preparation. Tissue Antigens 81:141–149

    Article  CAS  PubMed  Google Scholar 

  38. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, et al. (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. (2009) Introducing mothur: open-source platform-independent community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75:7537–7541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl. Environ. Microbiol. 79:5112–5120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Ter Braak CJF, Šmilauer P (2002) CANOCO reference manual and CanoDraw for Windows user’s guide: software for canonical community ordination (version 4.5). Microcomputer Power, Ithaca

  43. Coleman-Derr D, Desgarennes D, Fonseca-Garcia C, Gross S, Clingenpeel S, Woyke T, et al. (2015) Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species. New Phytol doi. doi:10.1111/nph.13697

    Google Scholar 

  44. Nekola JC, White PS (1999) The distance decay of similarity in biogeography and ecology. J. Biogeogr. 26:867–878

    Article  Google Scholar 

  45. Burgsdorf I, Erwin PM, López-Legentil S, Cerrano C, Haber M, Frenk S, et al. (2014) Biogeography rather than association with cyanobacteria structures symbiotic microbial communities in the marine sponge Petrosia ficiformis. Front. Microbiol. 5:529

    Article  PubMed  PubMed Central  Google Scholar 

  46. Finkel OM, Burch AY, Lindow SE, Post AF, Belkin S (2011) Phyllosphere microbial communities of a salt-excreting desert tree: geographical location determines population structure. Appl. Environ. Microbiol. 21:7647–7655

    Article  Google Scholar 

  47. Hazard C, Gosling P, Van Der Gast CJ, Mitchell DT, Doohan FM, Bending GD (2013) The role of local environment and geographical distance in determining community composition of arbuscular mycorrhizal fungi at the landscape scale. ISME J 7:498–508

    Article  CAS  PubMed  Google Scholar 

  48. Ferrenberg S, O’Neill SP, Knelman JE, Todd B, Duggan S, Bradley D, et al. (2013) Changes in assembly processes in soil bacterial communities following a wildfire disturbance. ISME J 7:1102–1111

    Article  PubMed  PubMed Central  Google Scholar 

  49. Yom-Tov Y, Tchernov E (1988) The zoogeography of Israel: the distribution and abundance at a zoogeographical crossroad. Dortrecht, Boston, Lancaster

  50. Yannarell AC, Triplett EW (2005) Geographic and environmental sources of variation in lake bacterial community composition. Appl. Environ. Microbiol. 71:227–239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Nicholson SW, Thornburg R (2007) Nectar chemistry. In: Nicholson SW, Nepi M, Pacini E (eds) Nectaries and nectar. Springer, Berlin, pp. 215–264

    Chapter  Google Scholar 

  52. Mittelbach M, Yurkov AM, Nocentini D, Nepi M, Weigend M, Begerow D (2015) Nectar sugars and bird visitation define a floral niche for basidiomycetous yeast on the Canary Islands. BMC Ecol. 15:2–14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We would like to thank the three anonymous reviewers for their helpful comments and Adi Halpern for her assistance in generating the figures. This study was supported by grants from the Israel Science Foundation (ISF, grants no. 189/08, 1094/12, and 296/16).

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Authors and Affiliations

  1. Department of Evolutionary and Environmental Biology, Faculty of Natural Sciences, University of Haifa, Mount Carmel, Haifa, Israel

    Yana Aizenberg-Gershtein, Ido Izhaki & Malka Halpern

  2. Department of Biology and Environment, Faculty of Natural Sciences, University of Haifa, Oranim, Tivon, Israel

    Malka Halpern

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  1. Yana Aizenberg-Gershtein
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  2. Ido Izhaki
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  3. Malka Halpern
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Correspondence to Malka Halpern.

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Aizenberg-Gershtein, Y., Izhaki, I. & Halpern, M. From Microhabitat of Floral Nectar Up to Biogeographic Scale: Novel Insights on Neutral and Niche Bacterial Assemblies. Microb Ecol 74, 128–139 (2017). https://doi.org/10.1007/s00248-017-0935-9

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