Skip to main content

Advertisement

Log in

Red Mangrove Propagule Bacterial Communities Vary With Geographic, But Not Genetic Distance

  • Plant Microbe Interactions
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Bacterial communities associated with plant propagules remain understudied, despite the opportunities that propagules represent as dispersal vectors for bacteria to new sites. These communities may be the product of a combination of environmental influence and inheritance from parent to offspring. The relative role of these mechanisms could have significant implications for our understanding of plant–microbe interactions. We studied the correlates of microbiome community similarities across an invasion front of red mangroves (Rhizophora mangle L.) in Florida, where the species is expanding northward. We collected georeferenced propagule samples from 110 individuals of red mangroves across 11 populations in Florida and used 16S rRNA gene (iTag) sequencing to describe their bacterial communities. We found no core community of bacterial amplicon sequence variants (ASVs) across the Florida range of red mangroves, though there were some ASVs shared among individuals within most populations. Populations differed significantly as measured by Bray–Curtis dissimilarity, but not Unifrac distance. We generated data from 6 microsatellite loci from 60 individuals across 9 of the 11 populations. Geographic distance was correlated with beta diversity, but genetic distance was not. We conclude that red mangrove propagule bacterial communities are likely influenced more by local environmental acquisition than by inheritance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data Availability

The datasets generated during and/or analyzed during the current study will be available in the NCBI SRA Database repository under submission numbers PRJNA844062 and PRJNA842720 upon acceptance of publication. [https://www.ncbi.nlm.nih.gov/sra/PRJNA844062, https://www.ncbi.nlm.nih.gov/sra/PRJNA842720].

References

  1. Berg G, Rybakova D, Grube M, Köberl M (2016) The plant microbiome explored: implications for experimental botany. J Exp Bot 67:995–1002. https://doi.org/10.1093/jxb/erv466

    Article  CAS  PubMed  Google Scholar 

  2. Rodríguez CE, Antonielli L, Mitter B et al (2020) Heritability and functional importance of the setaria viridis bacterial seed microbiome. Phytobiomes J 4:40–52. https://doi.org/10.1094/PBIOMES-04-19-0023-R

    Article  Google Scholar 

  3. Hacquard S (2016) Disentangling the factors shaping microbiota composition across the plant holobiont. New Phytol 209(2):454–457

    Article  PubMed  Google Scholar 

  4. Zilber-Rosenberg I, Rosenberg E (2008) Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev 32:723–735. https://doi.org/10.1111/j.1574-6976.2008.00123.x

    Article  CAS  PubMed  Google Scholar 

  5. Tannenbaum I, Kaur J, Mann R et al (2020) Profiling the lolium perenne microbiome: from seed to seed. Phytobiomes J 4:281–289. https://doi.org/10.1094/PBIOMES-03-20-0026-R

    Article  Google Scholar 

  6. Compant S, Clément C, Sessitsch A (2010) Soil biology & biochemistry plant growth-promoting bacteria in the rhizo- and endosphere of plants : their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42(5):669–678. https://doi.org/10.1016/j.soilbio.2009.11.024

  7. Vokou D, Vareli K, Zarali E et al (2012) Exploring biodiversity in the bacterial community of the Mediterranean phyllosphere and its relationship with airborne bacteria. Microb Ecol 64:714–724. https://doi.org/10.1007/s00248-012-0053-7

    Article  PubMed  Google Scholar 

  8. Ul-Hasan S, Bowers RM, Figueroa-Montiel A et al (2019) Community ecology across bacteria, archaea and microbial eukaryotes in the sediment and seawater of coastal Puerto Nuevo, Baja California. PLoS One 14(2):e0212355

  9. Cope-Selby N, Cookson A, Squance M et al (2017) Endophytic bacteria in Miscanthus seed: implications for germination, vertical inheritance of endophytes, plant evolution and breeding. GCB Bioenergy 9:57–77. https://doi.org/10.1111/gcbb.12364

    Article  CAS  Google Scholar 

  10. Johnston-Monje D, Raizada MN (2011) Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography and ecology. PLoS ONE 6:e20396. https://doi.org/10.1371/journal.pone.0020396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Puente ME, Li CY, Bashan Y (2009) Endophytic bacteria in cacti seeds can improve the development of cactus seedlings. Environ Exp Bot 66:402–408. https://doi.org/10.1016/j.envexpbot.2009.04.007

    Article  CAS  Google Scholar 

  12. Puente ME, Li CY, Bashan Y (2009) Rock-degrading endophytic bacteria in cacti. Environ Exp Bot 66:389–401. https://doi.org/10.1016/j.envexpbot.2009.04.010

    Article  CAS  Google Scholar 

  13. Soldan R, Mapelli F, Crotti E et al (2019) Bacterial endophytes of mangrove propagules elicit early establishment of the natural host and promote growth of cereal crops under salt stress. Microbiol Res 223–225:33–43. https://doi.org/10.1016/j.micres.2019.03.008

    Article  CAS  PubMed  Google Scholar 

  14. Shade A, McManus PS, Handelsman J (2013) Unexpected diversity during community succession in the apple flower microbiome. MBio 4:e00602-12. https://doi.org/10.1128/mBio.00602-12

    Article  PubMed  PubMed Central  Google Scholar 

  15. Singh P, Santoni S, This P, Péros J-PP (2018) Genotype-environment interaction shapes the microbial assemblage in grapevine’s phyllosphere and carposphere: an NGS approach. Microorganisms 6:96. https://doi.org/10.3390/microorganisms6040096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Drexler JZ (2001) Maximum longevities of Rhizophora apiculata and R. mucronata propagules. Pacific Sci 55:17–22. https://doi.org/10.1353/psc.2001.0004

    Article  Google Scholar 

  17. Scherer B (2021) Patterns of bacterial community variation across anatomical, geographical, and genetic distance in Florida mangroves. Dissertation, Florida State University

  18. Duke NC, Ball MC, Ellison JC et al (2017) Factors influencing biodiversity and distributional gradients in mangroves. Biogeogr Lett 7:27–47

    Article  Google Scholar 

  19. Cavanaugh KC, Kellner JR, Forde AJ et al (2014) Poleward expansion of mangroves is a threshold response to decreased frequency of extreme cold events. Proc Natl Acad Sci U S A 111:723–727. https://doi.org/10.1073/pnas.1315800111

    Article  CAS  PubMed  Google Scholar 

  20. Koenig CC, Coleman FC, Eklund A-M et al (2007) Mangroves as essential nursery habitat for Goliath grouper (Epinephelus Itajara). Bull Mar Sci 80(3):567–585

  21. Norton SL, Wiley TR, Carlson JK et al (2012) Designating critical habitat for juvenile endangered smalltooth sawfish in the United States. Mar Coast Fish 4:473–480. https://doi.org/10.1080/19425120.2012.676606

    Article  Google Scholar 

  22. Morrissey JF, Gruber SH (1993) Habitat selection by juvenile lemon sharks, Negaprion brevirostris. Environ Biol Fishes 38:311–319. https://doi.org/10.1007/BF00007524

    Article  Google Scholar 

  23. Hodel RGJ, De Souza Cortez MB, Soltis PS, Soltis DE (2016) Comparative phylogeography of black mangroves (Avicennia germinans) and red mangroves (Rhizophora mangle) in Florida: testing the maritime discontinuity in coastal plants. Am J Bot 103:730–739. https://doi.org/10.3732/ajb.1500260

    Article  CAS  PubMed  Google Scholar 

  24. Kennedy JP, Garavelli L, Truelove NK et al (2017) Contrasting genetic effects of red mangrove (Rhizophora mangle L.) range expansion along West and East Florida. J Biogeogr 44:335–347. https://doi.org/10.1111/jbi.12813

    Article  Google Scholar 

  25. Kennedy JP, Craig H, Jara-Cavieres A et al (2020) Multiplex microsatellite PCR panels for the neotropical red mangrove, Rhizophora mangle: combining efforts towards a cost-effective and modifiable tool to better inform conservation and management. Conserv Genet Resour 12:503–513. https://doi.org/10.1007/s12686-020-01138-8

    Article  Google Scholar 

  26. Moye ZD, Das CR, Tokman JI et al (2020) Treatment of fresh produce with a Salmonella-targeted bacteriophage cocktail is compatible with chlorine or peracetic acid and more consistently preserves the microbial community on produce. J Food Saf 40:e12763. https://doi.org/10.1111/jfs.12763

    Article  Google Scholar 

  27. Trudeau S, Thibodeau A, Côté JC et al (2020) Contribution of the broiler breeders’ fecal microbiota to the establishment of the eggshell microbiota. Front Microbiol 11:1–14. https://doi.org/10.3389/fmicb.2020.00666

    Article  Google Scholar 

  28. Herlemann DPR, Labrenz M, Jürgens K et al (2011) Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J 5:1571–1579. https://doi.org/10.1038/ismej.2011.41

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Illumina (2013) 16S metagenomic sequencing library. https://support.illumina.com/downloads/16s_metagenomic_sequencing_library_preparation.html. Accessed 10 Jan 2019

  30. Boylen E, Rideout J, Dillon M et al (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37:852–857

    Article  Google Scholar 

  31. Kearse M, Moir R, Wilson A et al (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649

    Article  PubMed  PubMed Central  Google Scholar 

  32. Geneious (2021) Analyzing microsatellite traces tutorial. https://www.geneious.com/tutorials/microsatellites/. Accessed 10 Jan 2019

  33. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  34. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Callahan BJ, McMurdie PJ, Rosen MJ et al (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13:581–583. https://doi.org/10.1038/nmeth.3869

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Yilmaz P, Parfrey LW, Yarza P et al (2014) The SILVA and “all-species living tree project (LTP)” taxonomic frameworks. Nucl Acids Res 42:D643–D648. https://doi.org/10.1093/nar/gkt1209

  37. Muthiah S, Corrada Bravo H (2020) Wrench: wrench normalization for sparse count data. R. Package version 1.8.0. https://github.com/HCBravoLab/Wrench

  38. Chen J (2018) GUniFrac: generalized UniFrac distances. R package version 1:1

    Google Scholar 

  39. Oksanen J (2013) vegan: community ecology package. R package version 2.5-7. https://CRAN.R-project.org/package=vegan

  40. Anderson MJ (2017) Permutational multivariate analysis of variance (PERMANOVA). Wiley statsref: Statistics Reference Online. Wiley, pp 1–15

  41. Bray JR, Curtis JT (1957) An ordination of upland forest communities of southern Wisconsin. Ecol Monogr 27:325–349

    Article  Google Scholar 

  42. Griffiths SM, Antwis RE, Lenzi L et al (2019) Host genetics and geography influence microbiome composition in the sponge Ircinia campana. J Anim Ecol 88:1684–1695. https://doi.org/10.1111/1365-2656.13065

    Article  PubMed  PubMed Central  Google Scholar 

  43. Parker KE, Ward JO, Eggleston EM et al (2020) Characterization of a thermally tolerant Orbicella faveolata reef in Abaco, The Bahamas. Coral Reefs 39:675–685. https://doi.org/10.1007/s00338-020-01948-0

    Article  Google Scholar 

  44. Suárez-Moo P, Lamelas A, Garcia-Bautista I et al (2020) Characterization of sediment microbial communities at two sites with low hydrocarbon pollution in the southeast Gulf of Mexico. PeerJ 8:1–23. https://doi.org/10.7717/peerj.10339

    Article  Google Scholar 

  45. Redford A, Bowers R, Knight R et al (2010) Variability in the distribution of bacteria on tree leaves. Environ Microbiol 12:2885–2893. https://doi.org/10.1111/j.1462-2920.2010.02258.x

    Article  PubMed  PubMed Central  Google Scholar 

  46. Nelson EB (2017) The seed microbiome: origins, interactions, and impacts. Plant Soil 422:1–28. https://doi.org/10.1007/s11104-017-3289-7

    Article  CAS  Google Scholar 

  47. Turner TR, James EK, Poole PS et al (2013) The plant microbiome. Genome Biol 14:209. https://doi.org/10.1186/gb-2013-14-6-209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Hodel RGJ, Chen S, Payton AC et al (2017) Adding loci improves phylogeographic resolution in red mangroves despite increased missing data: comparing microsatellites and RAD-Seq and investigating loci filtering. Sci Rep 7:1–14. https://doi.org/10.1038/s41598-017-16810-7

    Article  CAS  Google Scholar 

  49. Cregger MA, Veach AM, Yang ZK et al (2018) The Populus holobiont: dissecting the effects of plant niches and genotype on the microbiome. Microbiome 6:1–14. https://doi.org/10.1186/s40168-018-0413-8

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank the following individuals and organizations: Katelyn Desorcy-Scherer, Olivia Mason, Scott Steppan, Emily Lemmon, Sophie McCoy, Peter Beerli, Fritz Pichardo, Natasza Fontaine, Prashant Singh, Amber Brown, Steven Miller, Catalina Cuellar-Gempeler, Jackson Powell, Kevin Olson, Natali Ramirez-Bullon, Cheston Peterson, Brian Moe, Catelyn Snyder, the Apalachicola National Estuarine Reserve, the Florida Department of Environmental Protection, the FSU Coastal and Marine Lab, the FSU Department of Biological Sciences, the FSU Graduate School, FNPS, and FNPS Magnolia Chapter.

Funding

This work was supported by the Florida Native Plant Society (FNPS); FNPS Magnolia Chapter; Florida State University (FSU) Department of Biological Sciences; and the FSU Graduate School.

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Brendan Scherer. The first draft of the manuscript was written by Brendan Scherer, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Brendan P. Scherer.

Ethics declarations

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 298 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Scherer, B.P., Mast, A. Red Mangrove Propagule Bacterial Communities Vary With Geographic, But Not Genetic Distance. Microb Ecol 86, 1010–1022 (2023). https://doi.org/10.1007/s00248-022-02147-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-022-02147-w

Keywords

Navigation