1407Accesses
33Citations
9Altmetric
1Mention
Abstract
The phyllosphere presents a unique system of discrete and easily replicable surfaces colonized primarily by bacteria. However, the biogeography of bacteria in the phyllosphere is little understood, especially at small to intermediate scales. Bacterial communities on the leaves of 91 southern magnolia (Magnolia grandiflora) trees 1–452 m apart in a small forest plot were analyzed and fragments of the 16S ribosomal RNA (rRNA) gene sequenced using the Illumina platform. Assemblages were dominated by members of the Alphaproteobacteria, Bacteroidetes, and Acidobacteria. Patterns in community composition were measured by both relative abundance (theta) and presence-absence (Jaccard) dissimilarity metrics. Distance-based Moran’s eigenvector map analyses of the distance-decay relationship found a significant, positive relationship between each dissimilarity metric and significant eigenfunctions derived from geographic distance between trees, indicating trees that were closer together had more similar bacterial phyllosphere communities. Indirect gradient analyses revealed that several environmental parameters (canopy cover, tree elevation, and the slope and aspect of the ground beneath trees) were significantly related to multivariate ordination scores based on relative bacterial sequence abundances; however, these relationships were not significant when looking at the incidence of bacterial taxa. This suggests that bacterial growth and abundance in the phyllosphere is shaped by different assembly mechanisms than bacterial presence or absence. More broadly, this study demonstrates that the distance-decay relationship applies to phyllosphere communities at local scales, and that environmental parameters as well as neutral forces may both influence spatial patterns in the phyllosphere.
This is a preview of subscription content,log in via an institution to check access.
Access this article
Subscribe and save
- Get 10 units per month
- Download Article/Chapter or eBook
- 1 Unit = 1 Article or 1 Chapter
- Cancel anytime
Buy Now
Price includes VAT (Japan)
Instant access to the full article PDF.




Similar content being viewed by others
References
Vorholt JA (2012) Microbial life in the phyllosphere. Nat Rev Microbiol 10:828–840
Morris CE, Kinkel LL (2002) Fifty years of phyllosphere microbiology: significant contributions to research in related fields. In: Lindow SE, Hecht-Poinar EJ, Elliott V (eds) Phyllosphere microbiology. APS Press, St. Paul, MN, pp 365–375
Clayton MK, Hudelson BD (1995) Analysis of spatial patterns in the phyllosphere. In: Andrews JH, Hirano SS (eds) Microbial ecology of leaves. Springer, New York, pp 111–131
Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Princeton University Press, Princeton, NJ
Kim M, Singh D, Lai-Hoe A, Go R, Abdul Rahim R, Ainuddin AN et al (2012) Distinctive phyllosphere bacterial communities in tropical trees. Microb Ecol 63:674–681
Kembel SW, O’Connor TK, Arnold HK, Hubbell SP, Wright SJ, Green J (2014) Relationships between phyllosphere bacterial communities and plant functional traits in a neotropical forest. Proc Natl Acad Sci U S A 111:13715–13720
Andrews JH, Harris RF (2000) The ecology and biogeography of microorganisms on plant surfaces. Annu Rev Phytopathol 38:145–180
Green J, Bohannan BJM (2006) Spatial scaling of microbial biodiversity. Trends Ecol Evol 21:501–507
Redford AJ, Bowers RM, Knight R, Linhart Y, Fierer N (2010) The ecology of the phyllosphere: geographic and phylogenetic variability in the distribution of bacteria on tree leaves. Environ Microbiol 12:2885–2893
Finkel OM, Burch AY, Lindow SE, Post AF, Belkin S (2011) Geographical location determines the population structure in phyllosphere microbial communities of a salt-excreting desert tree. Appl Environ Microb 77:7647–7655
Finkel OM, Burch AY, Elad T, Huse SM, Lindow SE, Post AF, Belkin S (2012) Distance-decay relationships partially determine diversity patterns of phyllosphere bacteria onTamrix trees across the sonoran desert. Appl Environ Microb 78:6187–6193
Brewer JS (2001) Current and presettlement tree species composition of some upland forests in northern Mississippi. J Torrey Bot Soc 128:332–349
Hijmans RJ (2015) Raster: geographic data analysis and modeling. R package version 2.3-24.,http://CRAN.R-project.org/package=raster
Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2009) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microb 79:5112–5120
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 Microb 75:7537–7541
Schloss PD, Gevers D, Westcott SL (2011) Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 6:1–14
Yue JC, Clayton MK (2005) A similarity measure based on species proportions. Commun Stat-Theor M 34:2123–2131
R Core Team (2013) R: a language and environment for statistical computing. R Foundation for statistical Computing, Vienna, Austria,http://www.R-project.org/
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB et al (2015) Vegan: community ecology package. R package version 2.2-1.,http://CRAN.R-project.org/package=vegan
Legendre P, Borcard D, Blanchet FG, Dray S (2013) PCNM: MEM spatial eigenfunction and principal coordinate analyses. R package version 2.1-2/r109.,http://R-Forge.R-project.org/projects/sedar/
Legenre P, Fortin MJ, Borcard D (2015) Should the Mantel test be used in spatial analysis? Methods Ecol Evol: 1239–1247. Supplementary Information, Appendix S4, dbRDAF-test for response data in dissimilarity matrix form: 26–30
Jackson CR, Denney WC (2011) Annual and seasonal variation in the phyllosphere bacterial community associated with leaves of the southern magnolia (Magnolia grandiflora). Microb Ecol 61:113–122
Steppe K, Niinemets Ü, Teskey RO (2011) Tree size- and age-related changes in leaf phisiology and their influence on carbon gain. In: Meinzer FC, Lachenbruch B, Dawson TE (eds) Size-and age-related changes in tree structure and function. Springer, New York, NY, pp 235–254
Kinkel LE (1997) Microbial population dynamics on leaves. Annu Rev Phytopathol 35:327–347
Whipps JM, Hand P, Pink D, Bending GD (2008) Phyllosphere microbiology with special reference to diversity and plant genotype. J Appl Microbiol 105:1744–1755
Remus-Emsermann MNP, Tecon R, Kowalchuk GA, Leveau JHJ (2012) Variation in local carrying capacity and the individual fate of bacterial colonizers in the phyllosphere. ISME J 6:756–765
Lighthart B (1997) The ecology of bacteria in the alfresco atmosphere. FEMS Microbiol Ecol 23:263–274
Brandao PFB, Clapp JP, Bull AT (2002) Discrimination and taxonomy of geographically diverse strains of nitrile-metabolizing actinomycetes using chemometric and molecular sequencing techniques. Environ Microbiol 4:262–276
Horner-Devine MC, Lage M, Hughes JB, Bohannan BJM (2004) A taxa-area relationship for bacteria. Nature 432:750–753
Galand PE, Casamayor EO, Kirchman DL, Lovejoy C (2009) Ecology of the rare microbial biosphere of the Arctic Ocean. Proc Natl Acad Sci U S A 106:22427–22432
Whitaker RJ, Grogan DW, Taylor JW (2003) Geographic barriers isolate endemic populations of hyperthermophilic archaea. Science 301:976–978
Papke RT, Ramsing NB, Bateson MM, Ward DM (2003) Geographical isolation in hot spring cyanobacteria. Environ Microbiol 5:650–659
Martiny JBH, Bohannan BJM, Brown JH, Colwell RK, Fuhrman JA, Green JL et al (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4:102–112
Bell T (2010) Experimental tests of the bacterial distance-decay relationship. ISME J 4:1357–1365
Meyer KM, Leveau JHJ (2012) Microbiology of the phyllosphere: a playground for testing ecological concepts. Oecologia 168:621–629
Acknowledgments
We thank Heather Valdin and Jennifer Bell for help with the collection and processing of samples.
Sequence data
The nucleotide sequence data reported are available in the SRA database under the project accession number PRJNA293874.
Author information
Authors and Affiliations
Department of Biology, University of Mississippi, Shoemaker Hall, University MS, P.O. Box 1848, Oxford, MS, 38677, USA
Bram W. G. Stone & Colin R. Jackson
- Bram W. G. Stone
You can also search for this author inPubMed Google Scholar
- Colin R. Jackson
You can also search for this author inPubMed Google Scholar
Corresponding author
Correspondence toBram W. G. Stone.
Ethics declarations
Conflict of Interest
The authors declare that they have no conflict of interests.
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
Figure S1: Histograms of theta and Jaccard pairwise dissimilarities of bacterial phyllosphere communities grouped as dissimilarities between leaves on differentMagnolia grandiflora trees (top row) and dissimilarities between leaves on the same tree (bottom row). Thebold lines represent group means. Within-tree pairwise dissimilarities were found to be significantly lower using Monte Carlo randomization of thet statistic (ttheta = 8.67,p < 0.001 andtJaccard = 2.56,p < 0.001). (PDF 5 kb)
ESM 2
Figure S2: Bar chart of numbers of 16S bacterial sequence reads obtained from the leaves of each of 91Magnolia grandiflora trees. Off-target reads and artifacts from amplification and sequencing have been removed.Bars are divided andcolored by the eight most abundant bacterial phyla (read from the bottom up on the legend, i.e., beginning with the Proteobacteria). Thetop row indicates total sequence reads attributed to each tree (totaling to 7,025,849 bacterial sequences across the dataset), while the bottom row indicates the number of unique sequence reads attributed to each tree. Across the dataset, there were 20,416 unique bacterial sequences.Numbers along the horizontal axis indicate tree number (from 2 to 100), based on 100 trees initially sampled and 9 were removed due to low sequence coverage (less than 10,000 sequence reads) (PDF 13 kb)
ESM 3
(PDF 412 kb)
ESM 4
(PDF 81 kb)
ESM 5
(XLSX 20 kb)
Rights and permissions
About this article
Cite this article
Stone, B.W.G., Jackson, C.R. Biogeographic Patterns Between Bacterial Phyllosphere Communities of the Southern Magnolia (Magnolia grandiflora) in a Small Forest.Microb Ecol71, 954–961 (2016). https://doi.org/10.1007/s00248-016-0738-4
Received:
Accepted:
Published:
Issue Date:
Share this article
Anyone you share the following link with will be able to read this content:
Sorry, a shareable link is not currently available for this article.
Provided by the Springer Nature SharedIt content-sharing initiative