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Intraspecific variation on epiphytic bacterial community from Laguncularia racemosa phylloplane

  • Environmental Microbiology - Research Paper
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Abstract

Mangroves are dynamic and unique ecosystems that provide important ecological services to coastal areas. The phylloplane is one of the greatest microbial habitats, and most of its microorganisms are uncultivated under common laboratory conditions. Bacterial community structure of Laguncularia racemosa phylloplane, a well-adapted mangrove species with salt exudation at foliar levels, was accessed through 16S rRNA amplicon sequencing. Sampling was performed in three different sites across a transect from upland to the seashore in a preserved mangrove forest located in the city of Cananéia, São Paulo State, Brazil. Higher bacterial diversity was observed in intermediary locations between the upland and the seashore, showing that significant intraspecific spatial variation in bacterial communities exists between a single host species with the selection of specific population between an environmental transect.

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References

  1. Holguin G, Guzman MA, Bashan Y (1992) Two new nitrogen-fixing bacteria from the rhizosphere of mangrove trees : their isolation , identification and in vitro interaction with rhizosphere Staphylococcus sp. FEMS Microbiol Ecol 101(3):207–216

    Google Scholar 

  2. Baskaran R, Mohan P, Sivakumar K, Ragavan P, Sachithanandam V (2012) Phyllosphere microbial populations of ten true mangrove species of the Andaman Island. Int J Microbiol Res [Internet] 3(26):124–127 Available from: http://idosi.org/ijmr/ijmr3(2)12/8.pdf

    Google Scholar 

  3. Holguin G, Vazquez P, Bashan Y (2001) The role of sediment microorganisms in the productivity, conservation, and rehabilitation of mangrove ecosystems: an overview. Biol Fertil Soils 33(4):265–278

    CAS  Google Scholar 

  4. Wen M, Lin X, Xie M, Wang Y, Shen X, Liufu Z, Wu CI, Shi S, Tang T (2016) Small RNA transcriptomes of mangroves evolve adaptively in extreme environments. Sci Rep [Internet] 6:1–12. Available from:. https://doi.org/10.1038/srep27551

    Article  CAS  Google Scholar 

  5. Sobrado MA (2004) Influence of external salinity on the osmolality of xylem sap , leaf tissue and leaf gland secretion of the mangrove Laguncularia racemosa ( L .). Gaertn Trees 18(4):422–427

  6. Iermak I, Vink J, Bader AN, Wientjes E, Van Amerongen H (2016) Visualizing heterogeneity of photosynthetic properties of plant leaves with two-photon fluorescence lifetime imaging microscopy. Biochim Biophys Acta - Bioenerg 1857(9):1473–1478. Available from: https://doi.org/10.1016/j.bbabio.2016.05.005

    CAS  Google Scholar 

  7. Díaz S, Kattge J, Cornelissen JHC, Wright IJ, Lavorel S, Dray S, Reu B, Kleyer M, Wirth C, Colin Prentice I, Garnier E, Bönisch G, Westoby M, Poorter H, Reich PB, Moles AT, Dickie J, Gillison AN, Zanne AE, Chave J, Joseph Wright S, Sheremet’ev SN, Jactel H, Baraloto C, Cerabolini B, Pierce S, Shipley B, Kirkup D, Casanoves F, Joswig JS, Günther A, Falczuk V, Rüger N, Mahecha MD, Gorné LD (2015) The global spectrum of plant form and function. Nature [Internet] 529(7585):1–17. Available from:. https://doi.org/10.1038/nature16489

    Article  CAS  Google Scholar 

  8. Hacquard S, Spaepen S, Garrido-Oter R, Schulze-Lefert P (2017) Interplay between innate immunity and the plant microbiota. Annu Rev Phytopathol [Internet] 55(1):565–589. Available from:. https://doi.org/10.1146/annurev-phyto-080516-035623

    Article  CAS  Google Scholar 

  9. Vorholt JA (2012) Microbial life in the phyllosphere. Nat Publ Gr [Internet] 10(12):828–840. Available from:. https://doi.org/10.1038/nrmicro2910

    Article  CAS  Google Scholar 

  10. Lindow SE, Brandl MT (2003) Microbiology of the phyllosphere MINIREVIEW microbiology of the phyllosphere. Appl Environ Microbiol 69(4):1875–1883

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Bringel F (2015) Pivotal roles of phyllosphere microorganisms at the interface between plant functioning and atmospheric trace gas dynamics. Front Microbiol 6(May):1–14

    Google Scholar 

  12. Ryffel F, Helfrich EJN, Kiefer P, Peyriga L, Portais JC, Piel J, Vorholt JA (2016) Metabolic footprint of epiphytic bacteria on Arabidopsis thaliana leaves. ISME J 10(3):632–643

    CAS  PubMed  Google Scholar 

  13. Karamanoli K, Menkissoglu-Spiroudi U, Bosabalidis AM, Vokou D, Constantinidou HIA (2005) Bacterial colonization of the phyllosphere of nineteen plant species and antimicrobial activity of their leaf secondary metabolites against leaf associated bacteria. Chemoecology. 15(2):59–67

    Google Scholar 

  14. Laforest-Lapointe I, Messier C, Kembel SW (2016) Host species identity, site and time drive temperate tree phyllosphere bacterial community structure. Microbiome [Internet] 4:1–10. Available from:. https://doi.org/10.1186/s40168-016-0174-1

    Article  Google Scholar 

  15. Kembel SW, Connor TKO, Arnold HK, Hubbell SP, Wright SJ (2014) Relationships between phyllosphere bacterial communities and plant functional traits in a neotropical forest. PNAS. 111(38):13715–13720

    CAS  PubMed  Google Scholar 

  16. Lambais MR, Crowley DE, Cury JC, Bull RC, Rodrigues RR (2006) American Association for the Advancement of Science. Science (80- ) 312(5782):18–19

    Google Scholar 

  17. Müller T, Ruppel S (2014) Progress in cultivation-independent phyllosphere microbiology. FEMS Microbiol Ecol 87(1):2–17

    PubMed  Google Scholar 

  18. Peel MC, Finlayson BL, Mcmahon TA (2007) Updated world Koppen-Geiger climate classification map. Hydrol Earth Syst Sci 11:1633–1644

    Google Scholar 

  19. Sogin ML, Morrison HG, Huber JA, Mark Welch D, Huse SM, Neal PR, et al. Microbial diversity in the deep sea and the underexplored “rare biosphere”;. Proc Natl Acad Sci U S A [Internet] 2006;103(32):12115–12120. Available from: http://www.ncbi.nlm.nih.gov/pubmed/16880384%5Cn, http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC1524930

    CAS  Google Scholar 

  20. Wang Y, Sheng HF, He Y, Wu JY, Jiang YX, Tam NFY, Zhou HW (2012) Comparison of the levels of bacterial diversity in freshwater, intertidal wetland, and marine sediments by using millions of Illumina tags. Appl Environ Microbiol 78(23):8264–8271

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Moitinho MA, Bononi L, Souza DT, Melo IS, Taketani RG (2018) Bacterial succession decreases network complexity during plant material decomposition in mangroves. Microb Ecol 76(4):954–963

    CAS  PubMed  Google Scholar 

  22. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al (2010) Correspondence QIIME allows analysis of high- throughput community sequencing data intensity normalization improves color calling in SOLiD sequencing. Nat Publ Gr [Internet] 7(5):335–336. Available from:. https://doi.org/10.1038/nmeth0510-335

    Article  CAS  Google Scholar 

  23. R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing [Internet], Vienna, Austria Available from: http://www.r-project.org

    Google Scholar 

  24. McMurdie PJ, Holmes S (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8(4):e61217

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Love MI, Anders S, Huber W (2014) Differential analysis of count data - the DESeq2 package [Internet]. Genome Biol 15 550 p. Available from: https://doi.org/10.1101/002832%5Cnhttp://dx.doi.org/10.1186/s13059-014-0550-8

  26. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. United Kingdom: Journal of the Royal Statiscal Society (Series B). Wiley-Blackwell; 1995

    Google Scholar 

  27. Andreote FD, Jiménez DJ, Chavez D, Dias ACF, Luvizotto DM, Dini-Andreote F et al (2012) The microbiome of Brazilian mangrove sediments as revealed by metagenomics. PLoS One [Internet] 7(6):e38600. https://doi.org/10.1371/journal.pone.0038600 Available from: www.plosone.org

    Article  CAS  Google Scholar 

  28. Dias AC, Franco, Taketani RG, Andreote FD, Luvizotto DM, da Silva JL et al (2012) Interspecific variation of the bacterial community structure in the phyllosphere of. Brazilian J Microbiol 43(2):653–660

  29. Dos Santos HF, Cury JC, do Carmo FL, Dos Santos AL, Tiedje J, van Elsas JD et al (2011) Mangrove bacterial diversity and the impact of oil contamination revealed by pyrosequencing: bacterial proxies for oil pollution. PLoS One 6(3):1–8

    Google Scholar 

  30. Mendes LW, Tsai SM (2014) Variations of bacterial community structure and composition in mangrove sediment at different depths in Southeastern Brazil. Diversity. 6:827–843

    Google Scholar 

  31. Rigonato J, Alvarenga DO, Andreote FD, Cavalcante A, Dias F, Melo IS et al (2012) Cyanobacterial diversity in the phyllosphere of a mangrove forest. FEMS Microbiol Ecol 80:312–322

    CAS  PubMed  Google Scholar 

  32. Lynch JM, Whipps JM (1990) Substrate flow in the rhizosphere. Plant Soil 129:1–10

    CAS  Google Scholar 

  33. Ruiz-Pérez CA, Restrepo S, Zambrano MM (2016) Microbial and functional diversity within the phyllosphere of Espeletia species in an Andean high-mountain ecosystem. Appl Environ Microbiol 82(6):1807–1817

    PubMed  PubMed Central  Google Scholar 

  34. Bodenhausen N, Horton MW, Bergelson J (2013) Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. PLoS One 8(2):e56329

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Delmotte N, Knief C, Chaffron S, Innerebner G, Roschitzki B (2009) Schlapbach R. Community proteogenomics reveals insights into the physiology of phyllosphere bacteria, PNAS

    Google Scholar 

  36. Kim M, Singh D, Lai-Hoe A, Go R, Rahim RA, Ainuddin AN et al (2012) Distinctive phyllosphere bacterial communities in tropical trees. Microb Ecol 63(3):674–681

    PubMed  Google Scholar 

  37. Taketani RG, Franco NO, Rosado AS, van Elsas JD (2010) Microbial community response to a simulated hydrocarbon spill in mangrove sediments. J Microbiol [Internet] 48(1):7–15. Available from:. https://doi.org/10.1007/s12275-009-0147-1

    Article  Google Scholar 

  38. 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. Environ Microbiol 12:2885–2893

    PubMed  PubMed Central  Google Scholar 

  39. Lovelock CE, Feller IC, McKee KL, Thompson R (2005) Variation in mangrove forest structure and sediment characteristics in Bocas del Toro. Panama Caribb J Sci 41(3):456–464

    Google Scholar 

  40. Duke NC, Ball MC, Ellison JC (1998) Factors influencing biodiversity and distributional gradients in mangroves. Glob Ecol Biogeogr Lett 7(1):27–47

    Google Scholar 

  41. Leibold MA, Holyoak M, Mouquet N, Amarasekare P, Chase JM, Hoopes MF, Holt RD, Shurin JB, Law R, Tilman D, Loreau M, Gonzalez A (2004) The metacommunity concept: a framework for multi-scale community ecology. Ecol Lett 7(7):601–613

    Google Scholar 

  42. Bulgarelli D, Schlaeppi K, Spaepen S, Ver Loren van Themaat E, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol [internet] 64:807–838 Available from: http://www.ncbi.nlm.nih.gov/pubmed/23373698

    CAS  Google Scholar 

  43. Vokou D, Vareli K, Zarali E, Karamanoli K, Constantinidou HIA, Monokrousos N, Halley JM, Sainis I (2012) Exploring biodiversity in the bacterial community of the Mediterranean phyllosphere and its relationship with airborne bacteria. Microb Ecol 64(3):714–724

    PubMed  Google Scholar 

  44. Redford AJ, Bowers RM, Knight R, Linhart Y, Fierer N (2011) Variability in the distribution of bacteria on tree leaves. Environ Microbiol 12(11):2885–2893

    Google Scholar 

  45. Gomes NCM, Borges LR, Paranhos R, Pinto FN, Leda CS (2008) Exploring the diversity of bacterial communities in sediments of urban mangrove forests. FEMS Microbiol Ecol 66(2006):96–109

    CAS  Google Scholar 

  46. Geyer W (2010) Estuarine salinity structure and circulation. In: Valle-Levinson A (ed) Contemporary Issues in Estuarine Physics (pp. 12-26). Cambridge: Cambridge University Press. https://doi.org/10.1017/CBO9780511676567.003

  47. Cunha-Lignon M (2001) Dinâmica do manguezal no Sistema de Cananéia-Iguape, Estado de São Paulo – Brasil. Acta Bot Brasilica 15(2):56

    Google Scholar 

  48. Levin LA, Boesch DF, Covich A, Dahm C, Erséus C, Ewel KC, Kneib RT, Moldenke A, Palmer MA, Snelgrove P, Strayer D, Weslawski JM (2001) The function of marine critical transition zones and the importance of sediment biodiversity. Ecosystems. 4(5):430–451

    CAS  Google Scholar 

  49. Soares Júnior FL, Dias ACF, Fasanella CC, Taketani RG, de Sousa Lima AO, Melo IS et al (2013) Endo-and exoglucanase activities in bacteria from mangrove sediment. Brazilian J Microbiol 44(3):969–976

    Google Scholar 

  50. Bouvier TC, Del Giorgio PA (2002) Compositional changes in free-living bacterial communities along a salinity gradient in two temperate estuaries. Limnol Oceanogr 47(2):453–470

    CAS  Google Scholar 

  51. Yang J, Ma L, Jiang H, Wu G, Dong H (2016) Salinity shapes microbial diversity and community structure in surface sediments of the Qinghai-Tibetan Lakes. Sci Rep [Internet] 6(1):25078 Available from: http://www.nature.com/articles/srep25078

    CAS  Google Scholar 

  52. Jiang H, Huang Q, Deng S, Dong H, Yu B (2010) Planktonic actinobacterial diversity along a salinity gradient of a river and five lakes on the Tibetan Plateau. Extremophiles. 14(4):367–376

    PubMed  Google Scholar 

  53. Dillon JG, Carlin M, Gutierrez A, Nguyen V, Mclain N (2013) Patterns of microbial diversity along a salinity gradient in the Guerrero Negro solar saltern , Baja CA Sur. Mexico Front Microbiol 4(December):1–13

    Google Scholar 

  54. Knief C, Ramette A, Frances L, Alonso-Blanco C, Vorholt JA (2010) Site and plant species are important determinants of the Methylobacterium community composition in the plant phyllosphere. ISME J [Internet] 4(6):719–728. Available from:. https://doi.org/10.1038/ismej.2010.9

    Article  CAS  Google Scholar 

  55. Hunter PJ, Hand P, Pink D, Whipps JM, Bending GD (2010) Both leaf properties and microbe-microbe interactions influence within-species variation in bacterial population diversity and structure in the lettuce (Lactuca species) phyllosphere. Appl Environ Microbiol 76(24):8117–8125

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Dini-andreote F, Stegen JC, Dirk J, Elsas V, Falcão J (2015) Disentangling mechanisms that mediate the balance between stochastic and deterministic processes in microbial succession. PNAS112(11):E1326–E1332

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Acknowledgments

The authors thank João Luiz da Silva from Environmental EMBRAPA for his incredible support in mangrove expeditions and samplings.

Funding

This study was financed by FAPESP’s Young Investigators grant (2013/03158-4). RGT received a Young investigator fellowship (2013/23470-2). MAM received a doctorate fellowship from CNPq. JHS received a Master’s fellowship from FAPESP (2015/23102-9).

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Authors and Affiliations

  1. Laboratory of Environmental Microbiology, Brazilian Agricultural Research Corporation, EMBRAPA Environment, SP 340. Highway-Km 127.5, Jaguariúna, SP, 13820-000, Brazil

    Marta A. Moitinho, Josiane B. Chiaramonte, Danilo T. Souza, Juanita H. Solano, Laura Bononi & Itamar S. Melo

  2. College of Agriculture Luiz de Queiroz, University of São Paulo, Pádua Dias Avenue, 11, Piracicaba, SP, 13418-900, Brazil

    Marta A. Moitinho, Josiane B. Chiaramonte, Juanita H. Solano, Laura Bononi & Rodrigo G. Taketani

  3. CETEM, Centre for Mineral Technology, MCTIC Ministry of Science, Technology, Innovation and Communication, Cidade Universitária, Av. Pedro Calmon, 900, Cidade Universitária, Ilha do Fundão, Rio de Janeiro, ZC 21941-908, Brazil

    Rodrigo G. Taketani

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  1. Marta A. Moitinho
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  2. Josiane B. Chiaramonte
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  3. Danilo T. Souza
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Correspondence to Rodrigo G. Taketani.

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Moitinho, M.A., Chiaramonte, J.B., Souza, D.T. et al. Intraspecific variation on epiphytic bacterial community from Laguncularia racemosa phylloplane. Braz J Microbiol 50, 1041–1050 (2019). https://doi.org/10.1007/s42770-019-00138-7

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