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Variation in the bacteriome of the tropical liverwort, Marchantia inflexa, between the sexes and across habitats

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Plant-microbe interactions impact ecosystem function through nutrient cycling, community interactions, and individual costs/benefits to the organisms involved. However, information on the establishment, diversity, and function of plant-microbe interactions remains limited, especially for non-vascular plants. We hypothesized that variation in the environment and sex of a host plant, impact the composition and diversity of associated microbial communities. To test this hypothesis, we characterized the bacteriome of the non-vascular plant, Marchantia inflexa, in both males and females across multiple habitats by targeted sequencing of the bacterial 16S rRNA gene. We describe the bacteriome for M. inflexa, and find that it is abundant and diverse, showing some similarities with other non-vascular plant lineages. Using these data, we detected a habitat specific component of the bacteriome, and sex differences in the bacteriome under common garden conditions. On the basis of known microbial functions, our analyses suggest that the specific taxonomic assemblages of bacteria detected in particular habitat types may serve functional roles; allowing plants to better acclimate to their local environment, and that sex differences in the bacteriome may correspond to subtle differences in the physiology and morphology of the sexes. Our initial characterization of variation in bacteriome composition of this tropical liverwort lineage provides valuable information for better understanding the patterns of plant-microbe interactions across land plants.

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  1. Agler MT, Ruhe J, Kroll S et al. (2016) Microbial hub taxa link host and abiotic factors to plant microbiome variation (MK Waldor, Ed,). PLoS Biol, 14, e1002352

  2. Ali Balkan M (2016) Sex-specific fungal communities of the Dioicous Moss Ceratodon purpureus. Thesis, Portland State University.

  3. Andrews S. (2010).  FastQC: a quality control tool for high throughput sequence data. Available online at:

  4. Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486

  5. Bischler H (1984) Marchantia L: the new world species (Bryophytorum bibliotheca, band 26). Lubrecht & Cramer Ltd, Port Jervis

  6. Björnsson L, Hugenholtz P, Tyson GW, Blackall LL (2002) Filamentous Chloroflexi (green non-sulfur bacteria) are abundant in wastewater treatment processes with biological nutrient removal. Microbiology 148:2309–2318

  7. Bowers RM, McLetchie S, Knight R, Fierer N (2011) Spatial variability in airborne bacterial communities across land-use types and their relationship to the bacterial communities of potential source environments. The ISME Journal 5:601–612

  8. Bragina A, Berg C, Berg G (2015) The core microbiome bonds the alpine bog vegetation to a transkingdom metacommunity. Mol Ecol 24:4795–4807

  9. Bragina A, Berg C, Cardinale M et al (2012) Sphagnum mosses harbour highly specific bacterial diversity during their whole lifecycle. The ISME journal 6:802–813

  10. Bragina A, Oberauner-Wappis L, Zachow C et al (2014) The sphagnum microbiome supports bog ecosystem functioning under extreme conditions. Mol Ecol 23:4498–4510

  11. Brzyski JR, Taylor W, McLetchie DN (2014) Reproductive allocation between the sexes, across natural and novel habitats, and its impact on genetic diversity. Evol Ecol 28:247–261

  12. Bulgarelli D, Rott M, Schlaeppi K et al (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95

  13. Caporaso JG, Kuczynski J, Stombaugh J et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

  14. Claus SP, Tsang TM, Wang Y et al (2008) Systemic multicompartmental effects of the gut microbiome on mouse metabolic phenotypes. Mol Syst Biol 4:219

  15. Delaux P-M, Séjalon-Delmas N, Bécard G et al (2013) Evolution of the plant–microbe symbiotic “toolkit.”. Trends Plant Sci 18:298–304

  16. DeLuca TH, Zackrisson O, Nilsson M-C, Sellstedt A (2002) Quantifying nitrogen-fixation in feather moss carpets of boreal forests. Nature 419:917–920

  17. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemistry bulletin 19:11–15

  18. During H, Tooren BF Van (1990) Bryophyte interactions with other plants. Bot J Linn Soc, 104, 79–98

  19. Erlacher A, Cernava T, Cardinale M et al (2015) Rhizobiales as functional and endosymbiontic members in the lichen symbiosis of Lobaria Pulmonaria L. Front Microbiol 6:53

  20. Ezenwa VO, Gerardo NM, Inouye DW, Medina M, Xavier JB (2012) Microbiology. Animal behavior and the microbiome. Science 338:198–199

  21. Fuerst JA, Sagulenko E (2011) Beyond the bacterium: planctomycetes challenge our concepts of microbial structure and function. Nature Reviews. Microbiology 9:403–413

  22. Gifford SM, Sharma S, Moran MA (2014) Linking activity and function to ecosystem dynamics in a coastal bacterioplankton community. Front Microbiol 5:185

  23. Goffinet B (2008) Bryophyte Biology (AJ Shaw, Ed,). Cambridge University Press., Cambridge

  24. Groen KE, Stieha CR, Crowley PH, McLetchie DN (2010) Sex-specific plant responses to light intensity and canopy openness: implications for spatial segregation of the sexes. Oecologia 162:561–570

  25. Haney CH, Samuel BS, Bush J, Ausubel FM (2015) Associations with rhizosphere bacteria can confer an adaptive advantage to plants. Nature Plants 1:150–151

  26. van der Heijden MGA, Hartmann M, Turnbaugh P et al (2016) Networking in the plant microbiome. PLoS Biol 14:e1002378

  27. Hooper LV, Midtvedt T, Gordon JI (2002) How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu Rev Nutr 22:283–307

  28. Jafari N, Behroozi R, Farajzadeh D, Farsi M, Akbari-Noghabi K (2014) Antibacterial activity of Pseudonocardia sp. JB05, a rare salty soil actinomycete against Staphylococcus aureus. Biomed Res Int.

  29. Juottonen H, Galand PE, Tuittila E-S et al (2005) Methanogen communities and bacteria along an ecohydrological gradient in a northern raised bog complex. Environ Microbiol 7:1547–1557

  30. Knack JJ, Wilcox LW, Delaus P-M et al (2015) Microbiomes of Streptophyte algae and bryophytes suggest that a functional suite of microbiota fostered plant colonization of land. Int J Plant Sci 176:405–420

  31. Koua FHM, Kimbara K, Tani A (2014) Bacterial-biota dynamics of eight bryophyte species from different ecosystems. Saudi Journal of Biological Sciences 22:204–210

  32. Lebeis SL (2014) The potential for give and take in plant-microbiome relationships. Front Plant Sci 5:287

  33. Lee KCY, Dunfield PF, Stott MB (2014) The phylum Armatimonadetes. In: The prokaryotes. Springer Berlin Heidelberg, Berlin, pp 447–458

  34. Lozupone CA, Lladser ME, Knights D, Stombaugh J, Knight R (2011) UniFrac: an effective distance metric for microbial community comparison. The ISME Journal 5133:169–172

  35. Lundberg DS, Lebeis SL, Paredes SH et al (2012) Defining the core Arabidopsis Thaliana root microbiome. Nature 488:86–90

  36. Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963

  37. Manter DK, Delgado JA, Holm DG, Stong RA (2010) Pyrosequencing reveals a highly diverse and cultivar-specific bacterial endophyte community in potato roots. Microb Ecol 60:157–166

  38. Marks RA, Burton JF, McLetchie DN (2016) Sex differences and plasticity in dehydration tolerance: insight from a tropical liverwort. Ann Bot 118:347–356

  39. McLetchie DN, Puterbaugh MN (2000) Population sex ratios, sex-specific clonal traits and tradeoffs among these traits in the liverwort Marchantia Inflexa. Oikos 90:227–237

  40. Naether A, Foesel BU, Naegele V et al (2012) Environmental factors affect Acidobacterial communities below the subgroup level in grassland and forest soils. Appl Environ Microbiol 78:7398–7406

  41. Newton GL, Buchmeier N, Fahey RC (2008) Biosynthesis and functions of mycothiol, the unique protective thiol of Actinobacteria. Microbiol Mol Biol Rev 72:471–494

  42. Ofek M, Voronov-Goldman M, Hadar Y, Minz D (2014) Host signature effect on plant root-associated microbiomes revealed through analyses of resident vs . Active communities. Environ Microbiol 16:2157–2167

  43. Opelt K, Berg G (2004) Diversity and antagonistic potential of bacteria associated with bryophytes from nutrient-poor habitats of the Baltic Sea coast. Appl Environ Microbiol 70:6569–6579

  44. Opelt K, Berg C, Schönmann S, Eberl L, Berg G (2007a) High specificity but contrasting biodiversity of sphagnum-associated bacterial and plant communities in bog ecosystems independent of the geographical region. The ISME Journal 1:502–516

  45. Opelt K, Chobot V, Hadacek F et al (2007b) Investigations of the structure and function of bacterial communities associated with sphagnum mosses. Environ Microbiol 9:2795–2809

  46. Panke-Buisse K, Poole AC, Goodrich JK, Ley RE, Kao-Kniffin J (2015) Selection on soil microbiomes reveals reproducible impacts on plant function. The ISME journal 9:980–989

  47. Proctor MCF, Oliver MJ, Wood AJ et al (2007) Desiccation-tolerance in bryophytes : a review desiccation-tolerance in bryophytes : a review. Bryologist 110:595–621

  48. Schlaeppi K, Dombrowski N, Oter RG, Ver Loren van Themaat E, Schulze-Lefert P (2014) Quantitative divergence of the bacterial root microbiota in Arabidopsis Thaliana relatives. Proc Natl Acad Sci, 111, 585–592

  49. Sessitsch A, Mitter B (2015) 21st century agriculture: integration of plant microbiomes for improved crop production and food security. Microb Biotechnol 8:32–33

  50. Thomas F, Hehemann J-H, Rebuffet E, Czjzek M, Michel G (2011) Environmental and gut Bacteroidetes: the food connection. Front Microbiol 2:93

  51. Turner TR, James EK, Poole PS (2013) The plant microbiome. Genome Biol 14:209–219

  52. Vandenkoornhuyse P, Quaiser A, Duhamel M, Le Van A, Dufresne A (2015) The importance of the microbiome of the plant holobiont. New Phytol 206:1196–1206

  53. Varga S, Vega-Frutis R, Kytöviita M-M (2013) Transgenerational effects of plant sex and arbuscular mycorrhizal symbiosis. New Phytol 199:812–821

  54. Vega-Frutis R, Guevara R (2009) Different arbuscular mycorrhizal interactions in male and female plants of wild Carica papaya L. Plant Soil 322:167–176

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This project was funded by the University of Kentucky Biology Department’s Ribble Mini Grant program. We thank the University of Kentucky, College of Agriculture, Food and Environment for greenhouse space; the Wildlife Section, Forestry Division, Ministry of Agriculture, Land and Marine Resources of Trinidad and Tobago for collection and export permits; the Water and Sewage Authority for access to the research sites; and Andrea and Darryl McLetchie for logistical support in Trinidad. We thank Cara Haney (UBC), Scott Hotaling, Andrea Sanchez, Carol Baskin, Jonathan Moore (UKY), and multiple anonymous reviewers for comments that improved the manuscript.

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Correspondence to Rose A. Marks.

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Data Accessibility

Sequence data have been deposited in the NCBI SRA database (accession numbers: SRR5429634-56). Environmental data is available on Figshare (DOI:

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Marks, R.A., Smith, J.J., Cronk, Q. et al. Variation in the bacteriome of the tropical liverwort, Marchantia inflexa, between the sexes and across habitats. Symbiosis 75, 93–101 (2018).

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  • 16S sequencing
  • Marchantia inflexa
  • Microbiome
  • Sex differences