Microbial Ecology

, Volume 75, Issue 1, pp 88–103 | Cite as

Extensive Overlap of Tropical Rainforest Bacterial Endophytes between Soil, Plant Parts, and Plant Species

  • Emmanuel Haruna
  • Noraziah M. ZinEmail author
  • Dorsaf Kerfahi
  • Jonathan M. AdamsEmail author
Environmental Microbiology


The extent to which distinct bacterial endophyte communities occur between different plant organs and species is poorly known and has implications for bioprospecting efforts. Using the V3 region of the bacterial 16S ribosomal RNA (rRNA) gene, we investigated the diversity patterns of bacterial endophyte communities of three rainforest plant species, comparing leaf, stem, and root endophytes plus rhizosphere soil community. There was extensive overlap in bacterial communities between plant organs, between replicate plants of the same species, between plant species, and between plant organ and rhizosphere soil, with no consistent clustering by compartment or host plant species. The non-metric multidimensional scaling (NMDS) analysis highlighted an extensively overlapping bacterial community structure, and the β-nearest taxon index (βNTI) analysis revealed dominance of stochastic processes in community assembly, suggesting that bacterial endophyte operational taxonomic units (OTUs) were randomly distributed among plant species and organs and rhizosphere soil. Percentage turnover of OTUs within pairs of samples was similar both for plant individuals of the same species and of different species at around 80–90%. Our results suggest that sampling extra individuals, extra plant organs, extra species, or use of rhizosphere soil, might be about equally effective for obtaining new OTUs for culture. These observations suggest that the plant endophyte community may be much more diverse, but less predictable, than would be expected from culturing efforts alone.


Endophytes Metagenetics Rhizospheric bacteria Stochastic assembly Tropical rainforest plants 



We are grateful to the University Kebangsaan University Forest Reserve and Herbarium staff. We thank Muhanna Al-Shabanni, Aishah Ismail, Radhiah Binti Khairon, and Nur Faizah Abu Bakar, for their assistance during sampling. We thank Dr. Binu Tripathi for his contribution on the beta-NTI analysis. This work was funded by the Universiti Kebangsaan Malaysia Research Grant (GUP 2015-042).

Supplementary material

248_2017_1002_MOESM1_ESM.pdf (1.2 mb)
ESM 1 (PDF 1191 kb)


  1. 1.
    Ryan RP, Germaine K, Franks A, et al (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol. Lett. 278:1–9. doi: 10.1111/j.1574-6968.2007.00918.x PubMedCrossRefGoogle Scholar
  2. 2.
    Bodenhausen N, Horton MW, Bergelson J (2013) Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. PLoS One 8:e56329. doi: 10.1371/journal.pone.0056329 PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Sessitsch A, Hardoim P, Döring J, et al (2012) Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol. Plant-Microbe Interact. 25:28–36PubMedCrossRefGoogle Scholar
  4. 4.
    Kogel K-H, Franken P, Hückelhoven R (2006) Endophyte or parasite—what decides? Curr. Opin. Plant Biol. 9:358–363. doi: 10.1016/j.pbi.2006.05.001 PubMedCrossRefGoogle Scholar
  5. 5.
    Newton AC, Fitt BDL, Atkins SD, et al (2010) Pathogenesis, parasitism and mutualism in the trophic space of microbe-plant interactions. Trends Microbiol. 18:365–373. doi: 10.1016/j.tim.2010.06.002 PubMedCrossRefGoogle Scholar
  6. 6.
    van der Lelie D, Taghavi S, Monchy S, et al (2009) Poplar and its bacterial endophytes: coexistence and harmony. CRC Crit rev Plant Sci 28:346–358. doi: 10.1080/07352680903241204 CrossRefGoogle Scholar
  7. 7.
    Compant S, Clément C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol. Biochem. 42:669–678. doi: 10.1016/j.soilbio.2009.11.024 CrossRefGoogle Scholar
  8. 8.
    Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J. Microbiol. Biotechnol. 28:1327–1350. doi: 10.1007/s11274-011-0979-9 PubMedCrossRefGoogle Scholar
  9. 9.
    Baba MS, Zin NM, Hassan ZAA, et al (2015) In vivo antimalarial activity of the endophytic actinobacteria, Streptomyces SUK 10. J. Microbiol. 53:847–855. doi: 10.1007/s12275-015-5076-6 PubMedCrossRefGoogle Scholar
  10. 10.
    Yadav M, Yadav A, Kumar S, Yadav JP (2016) Spatial and seasonal influences on culturable endophytic mycobiota associated with different tissues of Eugenia jambolana Lam. and their antibacterial activity against MDR strains. BMC Microbiol. 16:44. doi: 10.1186/s12866-016-0664-0 PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Wani ZA, Ashraf N, Mohiuddin T, Riyaz-Ul-Hassan S (2015) Plant-endophyte symbiosis, an ecological perspective. Appl. Microbiol. Biotechnol. 99:2955–2965. doi: 10.1007/s00253-015-6487-3 PubMedCrossRefGoogle Scholar
  12. 12.
    Sarmin NIM, Zin NM, Tien NK, et al (2012) Ethnomedicinal plants as host of bioactive endophytic Actinomycetes. Sains Malaysiana 41:547–551Google Scholar
  13. 13.
    Jacobs MJ, Bugbee WM, Gabrielson DA (1985) Enumeration, location, and characterization of endophytic bacteria within sugar beet roots. Can. J. Bot. 63:1262–1265. doi: 10.1139/b85-174 CrossRefGoogle Scholar
  14. 14.
    Whitesides SK, Spotts RA (1991) Frequency, distribution, and characteristics of endophytic Pseudomonas syringe in pear trees. Phytopathology 81:453–457CrossRefGoogle Scholar
  15. 15.
    Brooks DS, Gonzalez CF, Appel DN, Filer TH (1994) Evaluation of endophytic bacteria as potential biological-control agents for oak wilt. Biol. Control 4:373–381. doi: 10.1006/bcon.1994.1047 CrossRefGoogle Scholar
  16. 16.
    Elbeltagy A, Nishioka K, Suzuki H, et al (2000) Isolation and characterization of endophytic bacteria from wild and traditionally cultivated rice varieties. Soil Sci Plant nu Tr 463:617–629. doi: 10.1080/00380768.2000.10409127 CrossRefGoogle Scholar
  17. 17.
    Zin N, Loi C, Sarmin N, Rosli A (2010) Cultivation-dependent characterization of endophytic Actinomycetes. Res. J. Microbiol. 5:717–724CrossRefGoogle Scholar
  18. 18.
    El-Deeb B, Bazaid S, Gherbawy Y, Elhariry H (2012) Characterization of endophytic bacteria associated with rose plant (Rosa damascena trigintipeta) during flowering stage and their plant growth promoting traits. J. Plant Interact. 7:248–253. doi: 10.1080/17429145.2011.637161 CrossRefGoogle Scholar
  19. 19.
    Ramond JB, Tshabuse F, Bopda CW, et al (2013) Evidence of variability in the structure and recruitment of rhizospheric and endophytic bacterial communities associated with arable sweet sorghum (Sorghum bicolor (L) Moench). Plant Soil 372:265–278. doi: 10.1007/s11104-013-1737-6 CrossRefGoogle Scholar
  20. 20.
    Edwards J, Johnson C, Santos-Medellín C, et al (2015) Structure, variation, and assembly of the root-associated microbiomes of rice. Proc. Natl. Acad. Sci. 112:E911–E920. doi: 10.1073/pnas.1414592112 PubMedCrossRefGoogle Scholar
  21. 21.
    Tian B-Y, Cao Y, Zhang K-Q, et al (2015) Metagenomic insights into communities, functions of endophytes, and their associates with infection by root-knot nematode, Meloidogyne incognita, in tomato roots. Sci rep 5:17087. doi: 10.1038/srep17087 PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Delmotte N, Knief C, Chaffron S, et al (2009) Community proteogenomics reveals insights into the physiology of phyllosphere bacteria. Proc. Natl. Acad. Sci. U. S. a. 106:16428–16433. doi: 10.1073/pnas.0905240106 PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Lundberg DS, Lebeis SL, Paredes SH, et al (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488:86–90. doi: 10.1038/nature11237 PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Bogas AC, Ferreira AJ, Araújo WL, et al (2015) Endophytic bacterial diversity in the phyllosphere of Amazon Paullinia cupana associated with asymptomatic and symptomatic anthracnose. Spring 4:258. doi: 10.1186/s40064-015-1037-0 CrossRefGoogle Scholar
  25. 25.
    Qin S, Chen H, Zhao G, et al (2012) Abundant and diverse endophytic actinobacteria associated with medicinal plant Maytenus austroyunnanensis in Xishuangbanna tropical rainforest revealed by culture-dependent and culture-independent methods. doi: 10.1111/j.1758-2229.2012.00357.x
  26. 26.
    Köberl M, Schmidt R, Ramadan EM, et al (2013) The microbiome of medicinal plants: diversity and importance for plant growth, quality, and health. 1219:54–51. doi:  10.3389/fmicb.2013.00400
  27. 27.
    Hao DC, Song SM, Mu J, et al (2016) Unearthing microbial diversity of Taxus rhizosphere via MiSeq high-throughput amplicon sequencing and isolate characterization. Sci rep 6:22006. doi: 10.1038/srep22006 PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Akinsanya MA, Goh JK, Lim SP, Ting ASY (2015) Diversity, antimicrobial and antioxidant activities of culturable bacterial endophyte communities in Aloe vera. FEMS Microbiol. Lett. 362:fnv184. doi: 10.1093/femsle/fnv184 PubMedCrossRefGoogle Scholar
  29. 29.
    Jin H, Yang XY, Yan ZQ, et al (2014) Characterization of rhizosphere and endophytic bacterial communities from leaves, stems and roots of medicinal Stellera chamaejasme L. Syst. Appl. Microbiol. 37:376–385. doi: 10.1016/j.syapm.2014.05.001 PubMedCrossRefGoogle Scholar
  30. 30.
    Montecchia MS, Tosi M, Soria MA, et al (2015) Pyrosequencing reveals changes in soil bacterial communities after conversion of Yungas forests to agriculture. PLoS One 10:e0119426. doi: 10.1371/journal.pone.0119426 PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Taketani R, Lima A, da Jesus E, C (2013) Bacterial community composition of anthropogenic biochar and Amazonian anthrosols assessed by 16S rRNA gene 454 pyrosequencing. Antonie van Leeuwenhoek 104:233–242Google Scholar
  32. 32.
    da Jesus E, C, Marsh T, Tiedje J (2009) Changes in land use alter the structure of bacterial communities in western Amazon soils. The ISME Journal 3:1004–1011Google Scholar
  33. 33.
    Lima A, Cannavan F, Navarrete A, Teixeira W (2015) Amazonian dark earth and plant species from the Amazon region contribute to shape rhizosphere bacterial communities. Microb. Ecol. 69:855–866CrossRefGoogle Scholar
  34. 34.
    Noyce G, Winsborough C, Fulthorpe R (2016) The microbiomes and metagenomes of forest biochars. Sci. Rep.Google Scholar
  35. 35.
    Sheng HM, Gao HS, Xue LG, et al (2011) Analysis of the composition and characteristics of culturable endophytic bacteria within subnival plants of the Tianshan Mountains, northwestern China. Curr. Microbiol. 62:923–932. doi: 10.1007/s00284-010-9800-5 PubMedCrossRefGoogle Scholar
  36. 36.
    Bulgari D, Casati P, Quaglino F, et al (2014) Endophytic bacterial community of grapevine leaves influenced by sampling date and phytoplasma infection process. BMC Microbiol. 14:198. doi: 10.1186/1471-2180-14-198 PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Carrell AA, Frank AC (2015) Bacterial endophyte communities in the foliage of coast redwood and giant sequoia. Front. Microbiol. doi: 10.3389/fmicb.2015.01008 PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Ulrich K, Ulrich A, Ewald D (2008) Diversity of endophytic bacterial communities in poplar grown under field conditions. FEMS Microbiol. Ecol. 63:169–180. doi: 10.1111/j.1574-6941.2007.00419.x PubMedCrossRefGoogle Scholar
  39. 39.
    Passari AK, Mishra VK, Saikia R, et al (2015) Isolation, abundance and phylogenetic affiliation of endophytic actinomycetes associated with medicinal plants and screening for their in vitro antimicrobial biosynthetic potential. Front. Microbiol. 6:1–13. doi: 10.3389/fmicb.2015.00273 CrossRefGoogle Scholar
  40. 40.
    Brader G, Compant S, Mitter B, et al (2014) Metabolic potential of endophytic bacteria. Curr. Opin. Biotechnol. 27:30–37. doi: 10.1016/j.copbio.2013.09.012 PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Strobel G, Daisy B (2003) Bioprospecting for microbial endophytes and their natural products. Microbiol. Mol. Biol. Rev. doi: 10.1128/MMBR.67.4.491-502.2003 PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Mousa WK, Raizada MN (2013) The diversity of anti-microbial secondary metabolites produced by fungal endophytes: an interdisciplinary perspective. Front. Microbiol. 4:65. doi: 10.3389/fmicb.2013.00065 PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Bhore S, Deivanai S, Bindusara A, Prabhakaran G (2014) Culturable bacterial endophytes isolated from mangrove tree (Rhizophora apiculata Blume) enhance seedling growth in Rice. J Nat Sci Biol med 5:437. doi: 10.4103/0976-9668.136233 PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Kusari S, Singh S, Jayabaskaran C (2014) Biotechnological potential of plant-associated endophytic fungi: hope versus hype. Trends Biotechnol. 32:297–303. doi: 10.1016/j.tibtech.2014.03.009 PubMedCrossRefGoogle Scholar
  45. 45.
    Laforest-Lapointe I, Messier C, Kembel SW, et al (2016) Host species identity, site and time drive temperate tree phyllosphere bacterial community structure. Microbiome 4:27. doi: 10.1186/s40168-016-0174-1 PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Kaul S, Sharma T, K Dhar M (2016) “Omics” tools for better understanding the plant-endophyte interactions. Front. Plant Sci. 7:955. doi:  10.3389/fpls.2016.00955
  47. 47.
    Rajasekaran D, Palombo EA, Yeo TC, et al (2013) Identification of traditional medicinal plant extracts with novel anti-influenza activity. PLoS One. doi: 10.1371/journal.pone.0079293 CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Ling SK, Tanaka T, Kouno I (2001) Iridoids from Rothmannia macrophylla. J. Nat. Prod. 64:796–798. doi: 10.1021/np000524c PubMedCrossRefGoogle Scholar
  49. 49.
    Chen Y-F, Huang Y, Tang W-Z, et al (2009) Antinociceptive activity of Paederosidic acid methyl Ester (PAME) from the n-butanol fraction of Paederia scandens in mice. Pharmacol. Biochem. Behav. 93:97–104. doi: 10.1016/j.pbb.2009.04.016 PubMedCrossRefGoogle Scholar
  50. 50.
    Beckers B, Op De Beeck M, Thijs S, et al (2016) Performance of 16s rDNA primer pairs in the study of rhizosphere and endosphere bacterial microbiomes in Metabarcoding studies. Front. Microbiol. 7:650. doi: 10.3389/fmicb.2016.00650 PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Huse SM, Dethlefsen L, Huber JA, et al (2008) Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genet. doi: 10.1371/journal.pgen.1000255 PubMedCrossRefPubMedCentralGoogle Scholar
  52. 52.
    Kerfahi D, Tripathi BM, Singh D, et al (2015) Effects of functionalized and raw multi-walled carbon nanotubes on soil bacterial community composition. PLoS One 10:e0123042. doi: 10.1371/journal.pone.0123042 PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Zhou H-W, Li D-F, Tam NF-Y, et al (2011) BIPES, a cost-effective high-throughput method for assessing microbial diversity. ISME j 5:741–749. doi: 10.1038/ismej.2010.160 PubMedCrossRefGoogle Scholar
  54. 54.
    Schloss PD, Westcott SL, Ryabin T, et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75:7537–7541. doi: 10.1128/AEM.01541-09 PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Masella AP, Bartram AK, Truszkowski JM, et al (2012) PANDAseq: paired-end assembler for illumina sequences. BMC Bioinformatics 13:31. doi: 10.1186/1471-2105-13-31 PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Chun J, Lee J, Jung Y, et al (2007) EzTaxon: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences, pp. 2259–2261. doi: 10.1099/ijs.0.64915-0 CrossRefGoogle Scholar
  57. 57.
    Huse SM, Welch DM, Morrison HG, Sogin ML (2010) Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ. Microbiol. 12:1889–1898. doi: 10.1111/j.1462-2920.2010.02193.x PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Schloss PD, Gevers D, Westcott SL (2011) Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. doi: 10.1371/journal.pone.0027310 CrossRefGoogle Scholar
  59. 59.
    Clarke K, Ainsworth M (1993) A method of linking multivariate community. Mar. Ecol. Prog. Ser. 92:205–219CrossRefGoogle Scholar
  60. 60.
    Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate—a practical and powerful approach to multiple testing. JRStatSocSerB StatMethodol 57:289–300Google Scholar
  61. 61.
    Dini-Andreote F, Stegen JC, van Elsas JD, Salles JF (2015) Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession. Proc. Natl. Acad. Sci. U. S. a. 112:E1326–E1332. doi: 10.1073/pnas.1414261112 PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Horner-Devine MC, Bohannan BJM (2006) Phylogenetic clustering and overdispersion in bacterial communities. Ecology 87:S100–S108PubMedCrossRefGoogle Scholar
  63. 63.
    Stegen JC, Lin X, Konopka AE, Fredrickson JK (2012) Stochastic and deterministic assembly processes in subsurface microbial communities. ISME j 6:1653–1664. doi: 10.1038/ismej.2012.22 PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Kembel SW, Hubbell SP (2006) The phylogenetic structure of a neotropical forest tree community. Ecology 87:S86–S99. doi: 10.1890/0012-9658(2006)87[86:TPSOAN]2.0.CO;2 PubMedCrossRefGoogle Scholar
  65. 65.
    Fine PVA, Kembel SW (2011) Phylogenetic community structure and phylogenetic turnover across space and edaphic gradients in western Amazonian tree communities. Ecography (cop) 34:552–565. doi: 10.1111/j.1600-0587.2010.06548.x CrossRefGoogle Scholar
  66. 66.
    Esty WW (1986) The efficiency of Good’s nonparametric coverage estimator. Ann. Stat. 14:1257–1260CrossRefGoogle Scholar
  67. 67.
    Otsuka S, Sudiana I, Komori A, et al (2008) Community structure of soil bacteria in a tropical rainforest several years after fire. Microbes Env 23:49–56. doi: 10.1264/jsme2.23.49 CrossRefGoogle Scholar
  68. 68.
    Lin Y-T, Huang Y-J, Tang S-L, et al (2010) Bacterial community diversity in undisturbed Perhumid montane Forest soils in Taiwan. Microb. Ecol. 59:369–378. doi: 10.1007/s00248-009-9574-0 PubMedCrossRefGoogle Scholar
  69. 69.
    Chan OC, Yang X, Fu Y, et al (2006) 16S rRNA gene analyses of bacterial community structures in the soils of evergreen broad-leaved forests in south-west China. FEMS Microbiol. Ecol. 58:247–259PubMedCrossRefGoogle Scholar
  70. 70.
    Tripathi BM, Kim M, Singh D, et al (2012) Tropical soil bacterial communities in Malaysia: pH dominates in the equatorial tropics too. Microb. Ecol. 64:474–484. doi: 10.1007/s00248-012-0028-8 PubMedCrossRefGoogle Scholar
  71. 71.
    Oh YM, Kim M, Lee-Cruz L, et al (2012) Distinctive bacterial communities in the rhizoplane of four tropical tree species. Microb. Ecol. 64:1018–1027. doi: 10.1007/s00248-012-0082-2 PubMedCrossRefGoogle Scholar
  72. 72.
    Tripathi BM, Song W, Slik JWF, et al (2016) Distinctive tropical forest variants have unique soil microbial communities, but not always low microbial diversity. Front. Microbiol. 7:1–11. doi: 10.3389/fmicb.2016.00376 CrossRefGoogle Scholar
  73. 73.
    Hu W, Zhang Q, Tian T, et al (2015) Relative roles of deterministic and stochastic processes in driving the vertical distribution of bacterial communities in a permafrost core from the Qinghai-Tibet plateau, China. PLoS One 10:1–19. doi: 10.1371/journal.pone.0145747 CrossRefGoogle Scholar
  74. 74.
    Wang J, Shen J, Wu Y, et al (2013) Phylogenetic beta diversity in bacterial assemblages across ecosystems: deterministic versus stochastic processes. ISME j 7:1310–1321. doi: 10.1038/ismej.2013.30 PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Rominger A, Miller T, Collins S (2009) Relative contributions of neutral and niche-based processes to the structure of a desert grassland grasshopper community. Oecologia 161:791–800PubMedCrossRefGoogle Scholar
  76. 76.
    Caruso T, Chan Y, Lacap DC, et al (2011) Stochastic and deterministic processes interact in the assembly of desert microbial communities on a global scale. ISME j 5:1406–1413. doi: 10.1038/ismej.2011.21 PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Wang J, Wu Y, Jiang H, et al (2008) High beta diversity of bacteria in the shallow terrestrial subsurface. Environ. Microbiol. 10:2537–2549PubMedCrossRefGoogle Scholar
  78. 78.
    Zhang X, Johnston ER, Liu W, et al (2016) Environmental changes affect the assembly of soil bacterial community primarily by mediating stochastic processes. Glob. Chang. Biol. 22:198–207. doi: 10.1111/gcb.13080 PubMedCrossRefGoogle Scholar
  79. 79.
    Hubbell SP (2001) The unified neutral theory of biodiversity and biogeography. Princeton University PressGoogle Scholar
  80. 80.
    Gentry AH (1988) Changes in plant community diversity and floristic composition on environmental and geographical gradients. Ann Missouri bot Gard 75:1–34. doi: 10.2307/2399464 CrossRefGoogle Scholar
  81. 81.
    Hollister EB, Engledow AS, Jo A, et al (2010) Shifts in microbial community structure along an ecological gradient of hypersaline soils and sediments. ISME j 4:829–838. doi: 10.1038/ismej.2010.3 PubMedCrossRefGoogle Scholar
  82. 82.
    Kembel SW, Mueller RC (2014) Plant traits and taxonomy drive host associations in tropical phyllosphere fungal communities. Botany 92:303–311. doi: 10.1139/cjb-2013-0194 CrossRefGoogle Scholar
  83. 83.
    Swenson N (2011) Deterministic tropical tree community turnover: evidence from patterns of functional beta diversity along an elevational gradient. Proc. R. Soc. Lond. B Biol. Sci. 278:877–884CrossRefGoogle Scholar
  84. 84.
    Condit R, Pitman N, Leigh E, Chave J (2002) Beta-diversity in tropical forest trees. Science 295(80):666–669. doi: 10.1126/science.1066854 PubMedCrossRefGoogle Scholar
  85. 85.
    Terborgh J (1992) Maintenance of diversity in tropical forests. Biotropica 24:283–292CrossRefGoogle Scholar
  86. 86.
    Ellwood F, Manica A, Foster W (2009) Stochastic and deterministic processes jointly structure tropical arthropod communities. Ecol. Lett. 12:227–284. doi: 10.1111/j.1461-0248.2009.01284.x CrossRefGoogle Scholar
  87. 87.
    Paquette A, Messier C (2011) The effect of biodiversity on tree productivity: from temperate to boreal forests. Glob. Ecol. Biogeogr. 20:170–180. doi: 10.1111/j.1466-8238.2010.00592.x CrossRefGoogle Scholar
  88. 88.
    Barbier S, Gosselin F, Balandier P (2008) Influence of tree species on understory vegetation diversity and mechanisms involved—a critical review for temperate and boreal forests. For. Ecol. Manag. 254:1–15CrossRefGoogle Scholar
  89. 89.
    Miyambo T, Makhalanyane TP, Cowan DA, Valverde A (2016) Plants of the fynbos biome harbour host species-specific bacterial communities. FEMS Microbiol. Lett. 363:fnw122. doi: 10.1093/femsle/fnw122 PubMedCrossRefGoogle Scholar
  90. 90.
    Carrell A, Carper D (2016) Subalpine conifers in different geographical locations host highly similar foliar bacterial endophyte communities. FEMS Microbiol. Ecol. 92:fiw124PubMedCrossRefGoogle Scholar
  91. 91.
    Ishida T, Nara K, Hogetsu T (2007) Host effects on ectomycorrhizal fungal communities: insight from eight host species in mixed conifer–broadleaf forests. New Phytol. 174:430–440PubMedCrossRefGoogle Scholar
  92. 92.
    Legendre P, Mi X, Ren H, et al (2009) Partitioning beta diversity in a subtropical broad-leaved forest of China. Ecology 90:663–674. doi: 10.1890/07-1880.1 PubMedCrossRefGoogle Scholar
  93. 93.
    Chase JM, Leibold MA (2003) Ecological niches: linking classical and contemporary approaches. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  94. 94.
    Vellend M, Srivastava DS, Anderson KM, et al (2014) Assessing the relative importance of neutral stochasticity in ecological communities. Oikos 123:1420–1430. doi: 10.1111/oik.01493 CrossRefGoogle Scholar
  95. 95.
    Karthikeyan B, Jaleel CA, Lakshmanan GMA, Deiveekasundaram M (2008) Studies on rhizosphere microbial diversity of some commercially important medicinal plants. Colloids Surfaces B Biointerfaces 62:143–145. doi: 10.1016/j.colsurfb.2007.09.004 PubMedCrossRefGoogle Scholar
  96. 96.
    Andreote FD, Azevedo JL, Araújo WL (2009) Assessing the diversity of bacterial communities associated with plants. Braz. J. Microbiol. 40:417–432. doi: 10.1590/S1517-83822009000300001 PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Li X, Rui J, Xiong J, et al (2014) Functional potential of soil microbial communities in the maize rhizosphere. PLoS One. doi: 10.1371/journal.pone.0112609 CrossRefPubMedPubMedCentralGoogle Scholar
  98. 98.
    Szymańska S, Płociniczak T, Piotrowska-Seget Z, Hrynkiewicz K (2016) Endophytic and rhizosphere bacteria associated with the roots of the halophyte Salicornia europaea L.—community structure and metabolic potential. Microbiol. Res. 192:37–51. doi: 10.1016/j.micres.2016.05.012 PubMedCrossRefGoogle Scholar
  99. 99.
    Costa R, Götz M, Mrotzek N, et al (2006) Effects of site and plant species on rhizosphere community structure as revealed by molecular analysis of microbial guilds. FEMS Microbiol. Ecol. 56:236–249. doi: 10.1111/j.1574-6941.2005.00026.x PubMedCrossRefGoogle Scholar
  100. 100.
    Coleman-Derr D, Desgarennes D, Fonseca-Garcia C, et al (2016) Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species. New Phytol. 209:798–811. doi: 10.1111/nph.13697 PubMedCrossRefGoogle Scholar
  101. 101.
    Bakker MG, Schlatter DC, Otto-Hanson L, Kinkel LL (2014) Diffuse symbioses: roles of plant-plant, plant-microbe and microbe-microbe interactions in structuring the soil microbiome. Mol. Ecol. 23:1571–1583. doi: 10.1111/mec.12571 PubMedCrossRefGoogle Scholar
  102. 102.
    Schlatter DC, Bakker MG, Bradeen JM, Kinkel LL (2015) Plant community richness and microbial interactions structure bacterial communities in soil. Ecology 96:134–142PubMedCrossRefGoogle Scholar
  103. 103.
    Makhalanyane TP, Valverde A, Gunnigle E, et al (2015) Microbial ecology of hot desert edaphic systems. FEMS Microbiol. Rev. 39:203–221. doi: 10.1093/femsre/fuu011 PubMedCrossRefGoogle Scholar
  104. 104.
    Jackson CR, Randolph KC, Osborn SL, et al (2013) Culture dependent and independent analysis of bacterial communities associated with commercial salad leaf vegetables. BMC Microbiol. 13:274. doi: 10.1186/1471-2180-13-274 PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Eevers N, Beckers B, Op de Beeck M, et al (2016) Comparison between cultivated and total bacterial communities associated with Cucurbita pepo using cultivation-dependent techniques and 454 pyrosequencing. Syst. Appl. Microbiol. 39:58–66. doi: 10.1016/j.syapm.2015.11.001 PubMedCrossRefGoogle Scholar
  106. 106.
    Qin S, Chen H-H, Zhao G-Z, et al (2012) Abundant and diverse endophytic actinobacteria associated with medicinal plant Maytenus austroyunnanensis in Xishuangbanna tropical rainforest revealed by culture-dependent and culture-independent methods. Environ. Microbiol. Rep. 4:522–531. doi: 10.1111/j.1758-2229.2012.00357.x PubMedCrossRefGoogle Scholar
  107. 107.
    Tian B-Y, Cao Y, Zhang K-Q (2015) Metagenomic insights into communities, functions of endophytes, and their associates with infection by root-knot nematode, Meloidogyne Incognita, in tomato roots. Sci rep 5:17087. doi: 10.1038/srep17087 PubMedPubMedCentralCrossRefGoogle Scholar
  108. 108.
    Liu Y, Li Y, Yao S, et al (2015) Diversity and distribution of endophytic bacterial community in the noni (Morinda citrifolia L.) plant. African J Microbiol res 9:1649–1657. doi: 10.5897/AJMR2015.7443 CrossRefGoogle Scholar
  109. 109.
    Maignien L, DeForce EA, Chafee ME, et al (2014) Ecological succession and stochastic variation in the assembly of Arabidopsis thaliana Phyllosphere communities. MBio 5:e00682–13-e00682–13. doi:  10.1128/mBio.00682-13
  110. 110.
    Gao C, Shi N-N, Chen L, et al (2016) Relationships between soil fungal and woody plant assemblages differ between ridge and valley habitats in a subtropical mountain forest. New Phytol. doi: 10.1111/nph.14287 CrossRefPubMedPubMedCentralGoogle Scholar
  111. 111.
    Kim M, Heo E, Kang H, Adams J (2013) Changes in soil bacterial community structure with increasing disturbance frequency. Microb. Ecol. 66:171–181. doi: 10.1007/s00248-013-0237-9 PubMedCrossRefGoogle Scholar
  112. 112.
    Wang Z-Q, He J, Su Y-X, et al (2006) Isolation and identification of Bacillus anthracis in an accidental case. Wei Sheng Wu Xue Bao 46:460–462PubMedGoogle Scholar
  113. 113.
    Patra G, Vaissaire J, Weber-Levy M, et al (1998) Molecular characterization of Bacillus strains involved in outbreaks of anthrax in France in 1997. J. Clin. Microbiol. 36:3412–3414PubMedPubMedCentralGoogle Scholar
  114. 114.
    Bhore S, Komathi V, Kandasamy K (2013) Diversity of endophytic bacteria in medicinally important nepenthes species. J Nat Sci Biol med 4:431. doi: 10.4103/0976-9668.117022 PubMedPubMedCentralCrossRefGoogle Scholar
  115. 115.
    Srinath R, Siva R, Babu S (2014) Bacillus anthracis-like strain-carrying P seudomonas FPVA gene occurs as endophyte in vegetables. J. Food Saf. 34:57–61. doi: 10.1111/jfs.12095 CrossRefGoogle Scholar
  116. 116.
    Polter SJ, Caraballo AA, Lee YP, et al (2015) Isolation, identification, whole-genome sequencing, and annotation of four Bacillus Species, B. anthracis RIT375, B. circulans RIT379, B. altitudinis RIT380, and B. megaterium RIT381, from internal stem tissue of the insulin plant Costus Igneus. Genome Announc. doi: 10.1128/genomeA.00847-15 CrossRefPubMedPubMedCentralGoogle Scholar
  117. 117.
    Hong Y, Liao D, Hu A, et al (2015) Diversity of endophytic and rhizoplane bacterial communities associated with exotic Spartina alterniflora and native mangrove using Illumina amplicon sequencing. Can. J. Microbiol. 61:723–733. doi: 10.1139/cjm-2015-0079 PubMedCrossRefGoogle Scholar
  118. 118.
    Choudhary DK, Johri BN (2009) Interactions of Bacillus spp. and plants—with special reference to induced systemic resistance (ISR). Microbiol. Res. 164:493–513. doi: 10.1016/j.micres.2008.08.007 PubMedCrossRefGoogle Scholar
  119. 119.
    Melnick RL, Zidack NK, Bailey BA, et al (2008) Bacterial endophytes: Bacillus spp. from annual crops as potential biological control agents of black pod rot of cacao. Biol. Control 46:46–56. doi: 10.1016/j.biocontrol.2008.01.022 CrossRefGoogle Scholar
  120. 120.
    Alina SO, Constantinscu F, Petruţa CC (2015) Biodiversity of Bacillus subtilis group and beneficial traits of Bacillus species useful in plant protection. Rom Biotechnol Lett 20:10737–10750Google Scholar
  121. 121.
    Nielsen DS, Kobawila SC, Anyogu A, et al (2015) Lysinibacillus louembei sp. nov., a spore-forming bacterium isolated from Ntoba Mbodi, alkaline fermented leaves of cassava from the Republic of the Congo. Int. J. Syst. Evol. Microbiol. 65:4256–4262. doi: 10.1099/ijsem.0.000570 PubMedCrossRefGoogle Scholar
  122. 122.
    Duan Y-Q, He S-T, Li Q-Q, et al (2013) Lysinibacillus tabacifolii sp. nov., a novel endophytic bacterium isolated from Nicotiana tabacum leaves. J. Microbiol. 51:289–294. doi: 10.1007/s12275-013-2338-z PubMedCrossRefGoogle Scholar
  123. 123.
    Gallegos-Monterrosa R, Maróti G, Bálint B, Kovács ÁT (2016) Draft genome sequence of the soil isolate Lysinibacillus fusiformis M5, a potential hypoxanthine producer. Genome Announc 4:e01272–e01216. doi: 10.1128/genomeA.01272-16 PubMedPubMedCentralCrossRefGoogle Scholar
  124. 124.
    Reghuvaran A, Jacob KK, Ravindranath AD (2012) Isolation and characterization of nitrogen fixing bacteria from raw coir pith. African J Biotechnol 11:7063–7071. doi: 10.5897/AJB11.2205 CrossRefGoogle Scholar
  125. 125.
    Vendan RT, Yu YJ, Lee SH, Rhee YH (2010) Diversity of endophytic bacteria in ginseng and their potential for plant growth promotion. J. Microbiol. 48:559–565. doi: 10.1007/s12275-010-0082-1 PubMedCrossRefGoogle Scholar
  126. 126.
    Salm JL, Baker MBJ, Beau CJ, Cuce J (2011) Anti-malarial activity exhibited by Florida mangrove endophytes. University of South Florida, FloridaGoogle Scholar
  127. 127.
    Santiago C, Sun L, Munro MHG, Santhanam J (2014) Polyketide and benzopyran compounds of an endophytic fungus isolated from Cinnamomum mollissimum: biological activity and structure. Asian Pac J Trop Biomed 4:627–632. doi: 10.12980/APJTB.4.2014APJTB-2014-0030 PubMedPubMedCentralCrossRefGoogle Scholar
  128. 128.
    Hu X, Fan W, Han B, et al (2008) Complete genome sequence of the mosquitocidal bacterium Bacillus sphaericus C3-41 and comparison with those of closely related Bacillus species. J. Bacteriol. 190:2892–2902. doi: 10.1128/JB.01652-07 PubMedPubMedCentralCrossRefGoogle Scholar
  129. 129.
    Kloepper JW, Ryu C-M, Zhang S (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259–1266. doi: 10.1094/PHYTO.2004.94.11.1259 PubMedCrossRefGoogle Scholar
  130. 130.
    Timmusk S, Wagner EGH (1999) The plant-growth-promoting Rhizobacterium Paenibacillus polymyxa induces changes in Arabidopsis thaliana gene expression: a possible connection between biotic and abiotic stress responses. Mol. Plant-Microbe Interact. 12:951–959. doi: 10.1094/MPMI.1999.12.11.951 PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  1. 1.Programme of Biomedical Science, School of Diagnostic and Applied Health Sciences, Faculty of Health SciencesUniversiti Kebangsaan MalaysiaKuala LumpurMalaysia
  2. 2.Department of BiochemistryKaduna State UniversityKadunaNigeria
  3. 3.Department of Biological SciencesSeoul National UniversitySeoulRepublic of Korea

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