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The role of macrophyte-associated microbiomes in lacustrine wetlands: an example of the littoral zone of lake Atitlan, Guatemala

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Abstract

Despite rapid progress in plant–microbe interaction research within terrestrial environments, our knowledge of aquatic plant and macroalgae microbiome structure, function, and ecology remains scarce, even though these hosts are key players in structuring the lacustrine environments. Here, we used the co-occurring, fast-growing hosts Hydrilla verticillata (Hydrocharitaceae) and Cladophora spp. (Chlorophyta), which dominate the littoral zones of a nitrogen-limited, hard-water lake, Lake Atitlán (Guatemala). The aim of this study was: (1) to assess the structure of Hydrilla phyllosphere-associated and Cladophora filament-associated bacterial and fungal assemblages in the context of host specificity; (2) to predict microbial potential to contribute to biogeochemical cycling in the lake littoral; and (3) to compare the aquatic microbiome structure to available datasets from terrestrial ecosystems, using next-generation amplicon sequencing, co-occurrence network analysis, and N2-fixation activity measurements. We show that the microbiomes associated with the phyllosphere of aquatic macrophytes and macroalgal filaments are surprisingly similar, with taxonomic and functional complexity analogous to that of rhizospheric assemblages in terrestrial plants, and have a potential to efficiently recycle nutrients from organic matter. We suggest that especially the fungal associations with these hosts represent an untapped research area of microbial ecology that warrants further attention.

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Data availability

Raw sequences of 16SrDNA and ITS1 amplicons were deposited in the European Nucleotide Archive (ENA) under the study ID PRJEB42360. All other data are available from the authors upon reasonable request.

References

  • Aßhauer, K. P., B. Wemheuer, R. Daniel & P. Meinicke, 2015. Tax4Fun: predicting functional profiles from metagenomic 16S rRNA data. Bioinformatics 31: 2882–2884.

    PubMed  PubMed Central  Google Scholar 

  • Ambus, P. & S. Zechmeister-Boltenstern, 2007. Denitrification and N-cycling in forest ecosystems. In Bothe, H., S. Ferguson & W. E. Newton (eds), Biology of the Nitrogen Cycle Elsevier, Amsterdam: 343–358.

    Google Scholar 

  • Angelstein, S. & H. Schubert, 2008. Elodea nuttallii: uptake, translocation and release of phosphorus. Aquatic Biology 3: 209–216.

    Google Scholar 

  • Ariosa, Y., A. Quesada, J. Aburto, D. Carrasco, R. Carreres, F. Leganés & E. F. Valiente, 2004. Epiphytic cyanobacteria on Chara vulgaris are the main contributors to N2 fixation in rice fields. Applied and Environmental Microbiology 70: 5391–5397.

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Bárta, J., K. Tahovská, H. Šantrůčková & F. Oulehle, 2017. Microbial communities with distinct denitrification potential in spruce and beech soils differing in nitrate leaching. Scientific Reports 7: 1–15.

    Google Scholar 

  • Bengtsson-Palme, J., M. Ryberg, M. Hartmann, S. Branco, Z. Wang, A. Godhe, P. De Wit, M. Sánchez-García, I. Ebersberger, F. de Sousa, A. Amend, A. Jumpponen, M. Unterseher, E. Kristiansson, K. Abarenkov, Y. J. K. Bertrand, K. Sanli, K. M. Eriksson, U. Vik, V. Veldre & R. H. Nilsson, 2013. Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data. Methods in Ecology and Evolution 4: 914–919.

    Google Scholar 

  • Benjamini, Y. & Y. Hochberg, 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B 57: 289–300.

    MathSciNet  Google Scholar 

  • Berg, G., M. Grube, M. Schloter & K. Smalla, 2014. Unraveling the plant microbiome: looking back and future perspectives. Frontiers in Microbiology 5: 148.

    PubMed  PubMed Central  Google Scholar 

  • Braus, M. J., L. E. Graham & T. L. Whitman, 2017. Spatiotemporal dynamics of the bacterial microbiota on lacustrine Cladophora glomerata (Chlorophyta). Journal of Phycology 53: 1255–1262.

    PubMed  Google Scholar 

  • Breinlinger, S., T. J. Phillips, B. N. Haram, J. Mareš, J. A. Martínez Yerena, P. Hrouzek, R. Sobotka, W. M. Henderson, P. Schmieder, S. M. Williams, J. D. Lauderdale, H. D. Wilde, W. Gerrin, A. Kust, J. W. Washington, C. Wagner, B. Geier, M. Liebeke, H. Enke, T. H. J. Niedermeyer & S. B. Wilde, 2021. Hunting the eagle killer: a cyanobacterial neurotoxin causes vacuolar myelinopathy. Science American Association for the Advancement of Science 371: eaax9050.

    CAS  Google Scholar 

  • Caporaso, J. G., J. Kuczynski, J. Stombaugh, K. Bittinger, F. D. Bushman, E. K. Costello, N. Fierer, A. G. Peña, J. K. Goodrich, J. I. Gordon, G. A. Huttley, S. T. Kelley, D. Knights, J. E. Koenig, R. E. Ley, C. A. Lozupone, D. McDonald, B. D. Muegge, M. Pirrung, J. Reeder, J. R. Sevinsky, P. J. Turnbaugh, W. A. Walters, J. Widmann, T. Yatsunenko, J. Zaneveld & R. Knight, 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7: 335–336.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Caporaso, J. G., C. L. Lauber, W. A. Walters, D. Berg-Lyons, C. A. Lozupone, P. J. Turnbaugh, N. Fierer & R. Knight, 2011. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proceedings of the National Academy of Sciences of the United States of America 108: 4516–4522.

    ADS  CAS  PubMed  Google Scholar 

  • Cardini, U., N. van Hoytema, V. N. Bednarz, M. M. D. Al-Rshaidat & C. Wild, 2018. N2 fixation and primary productivity in a red sea Halophila stipulacea meadow exposed to seasonality. Limnology and Oceanography 63: 786–798.

    ADS  CAS  Google Scholar 

  • Castro, W. A. C. D., R. C. Bonugli-Santos, A. C. Sibim, M. B. D. Cunha-Santino & I. Bianchini Jr., 2021. Enzymatic efficiency of the decomposing microbiota: what does really matter for aquatic macrophytes invasions? Acta Botanica Brasilica 35: 104–110.

    Google Scholar 

  • Chong, J., P. Liu, G. Zhou & J. Xia, 2020. Using MicrobiomeAnalyst for comprehensive statistical, functional, and meta-analysis of microbiome data. Nature Protocols 15: 799–821.

    CAS  PubMed  Google Scholar 

  • Cordovez, V., F. Dini-Andreote, V. J. Carrión & J. M. Raaijmakers, 2019. Ecology and evolution of plant microbiomes. Annual Review of Microbiology 73: 69–88.

    CAS  PubMed  Google Scholar 

  • Corman, J. R., E. Carlson, M. Dix, N. Girón, A. Roegner, J. Veselá, S. Chandra, J. J. Elser & E. Rejmánková, 2015. Nutrient dynamics and phytoplankton resource limitation in a deep tropical mountain lake. Inland Waters 5: 371–386.

    Google Scholar 

  • Cowardin, L. M., V. Carter, F. C. Golet & E. T. LaRoe, 1979. Classification of Wetlands and Deepwater Habitats of the United States, Fish and Wildlife Service Publishers, Washington:

    Google Scholar 

  • Craine, J. M., C. Morrow & N. Fierer, 2007. Microbial nitrogen limitation increases decomposition. Ecology 88: 2105–2113.

    PubMed  Google Scholar 

  • Crump, B. C. & E. W. Koch, 2008. Attached bacterial populations shared by four species of aquatic angiosperms. Applied and Environmental Microbiology 74: 5948–5957.

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Denny, P., 1972. Sites of nutrient absorption in aquatic macrophytes. The Journal of Ecology 60: 819–829.

    Google Scholar 

  • Ding, H., L. Lv, Z. Wang & L. Liu, 2020. Study on the “glutamic acid-enzymolysis” process for extracting chitin from crab shell waste and its by-product recovery. Applied Biochemistry and Biotechnology Springer 190: 1074–1091.

    CAS  Google Scholar 

  • Evangelista, H. B. A., S. M. Thomaz & C. A. Umetsu, 2014. An analysis of publications on invasive macrophytes in aquatic ecosystems. Aquatic Invasions 9: 521–528.

    Google Scholar 

  • Fish, J. A., B. Chai, Q. Wang, Y. Sun, C. T. Brown, J. M. Tiedje & J. R. Cole, 2013. FunGene: the functional gene pipeline and repository. Frontiers in Microbiology 4: 291.

    PubMed  PubMed Central  Google Scholar 

  • Furey, P. C., R. L. Lowe, M. E. Power & A. M. Campbell-Craven, 2012. Midges, Cladophora, and epiphytes: shifting interactions through succession. Freshwater Science North American Benthological Society 31: 93–107.

    Google Scholar 

  • Glöckner, F. O., M. Kube, M. Bauer, H. Teeling, T. Lombardot, W. Ludwig, D. Gade, A. Beck, K. Borzym, K. Heitmann, R. Rabus, H. Schlesner, R. Amann & R. Reinhardt, 2003. Complete genome sequence of the marine planctomycete Pirellula sp. strain 1. Proceedings of the National Academy of Sciences of the United States of America 100: 8298–8303.

    ADS  PubMed  PubMed Central  Google Scholar 

  • Gonzalez, A., J. A. Navas-Molina, T. Kosciolek, D. McDonald, Y. Vázquez-Baeza, G. Ackermann, J. DeReus, S. Janssen, A. D. Swafford, S. B. Orchanian, J. G. Sanders, J. Shorenstein, H. Holste, S. Petrus, A. Robbins-Pianka, C. J. Brislawn, M. Wang, J. R. Rideout, E. Bolyen, M. Dillon, J. G. Caporaso, P. C. Dorrestein & R. Knight, 2018. Qiita: rapid, web-enabled microbiome meta-analysis. Nature Methods 15: 796–798.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gooday, G. W., 1990. The ecology of chitin degradation. In Nelson, K. E. (ed), Advances in Microbial Ecology Springer, Boston: 387–430.

    Google Scholar 

  • Gounand, I., C. J. Little, E. Harvey & F. Altermatt, 2018. Cross-ecosystem carbon flows connecting ecosystems worldwide. Nature Communications 9: 1–8.

    CAS  Google Scholar 

  • Grossart, H. P., S. Van den Wyngaert, M. Kagami, C. Wurzbacher, M. Cunliffe & K. Rojas-Jimenez, 2019. Fungi in aquatic ecosystems. Nature Reviews Microbiology 17: 339–354.

    CAS  PubMed  Google Scholar 

  • Gu, B., 2006. Environmental conditions and phosphorus removal in Florida lakes and wetlands inhabited by Hydrilla verticillata (Royle): implications for invasive species management. Biological Invasions 8(7): 1569–1578.

    Google Scholar 

  • Hammer, Ø., D. A. Harper & P. D. Ryan, 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4: 9.

    Google Scholar 

  • Hardoim, P. R., L. S. Van Overbeek, G. Berg, A. M. Pirttilä, S. Compant, A. Campisano, M. Döring & A. Sessitsch, 2015. The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiology and Molecular Biology Reviews 79: 293–320.

    PubMed  PubMed Central  Google Scholar 

  • Harrison, J. G. & E. A. Griffin, 2020. The diversity and distribution of endophytes across biomes, plant phylogeny and host tissues: how far have we come and where do we go from here? Environmental Microbiology 22: 2107–2123.

    PubMed  PubMed Central  Google Scholar 

  • He, D., L. Ren & Q. L. Wu, 2014. Contrasting diversity of epibiotic bacteria and surrounding bacterioplankton of a common submerged macrophyte, Potamogeton crispus, in freshwater lakes. FEMS Microbiology 90: 551–562.

    CAS  Google Scholar 

  • Henneron, L., P. Kardol, D. A. Wardle, C. Cros & S. Fontaine, 2020. Rhizosphere control of soil nitrogen cycling: a key component of plant economic strategies. New Phytologist 228: 1269–1282.

    CAS  PubMed  Google Scholar 

  • Hilt, S., I. Henschke, J. Rücker & B. Nixdorf, 2010. Can submerged macrophytes influence turbidity and trophic state in deep lakes? Suggestions from a case study. Journal of Environmental Quality 39: 725–733.

    CAS  PubMed  Google Scholar 

  • Jackrel, S. L., S. M. Owens, J. A. Gilbert & C. A. Pfister, 2017. Identifying the plant-associated microbiome across aquatic and terrestrial environments: the effects of amplification method on taxa discovery. Molecular Ecology Resources 17: 931–942.

    CAS  PubMed  Google Scholar 

  • Jones, E. B. G. & R. Choeyklin, 2008. Ecology of marine and freshwater basidiomycetes. In Boddy, L., J. C. Frankland & P. West (eds), British Mycological Society Symposia Series Academic Press, London: 301–324.

    Google Scholar 

  • Kasana, R. C. & C. B. Pandey, 2018. Exiguobacterium: an overview of a versatile genus with potential in industry and agriculture. Critical Reviews in Biotechnology 38: 141–156.

    CAS  PubMed  Google Scholar 

  • Lahti, L., S. Shetty & T. Blake, 2017. Tools for microbiome analysis in R. Microbiome Package Version 0.99.

  • Langenheder, S. & E. S. Lindstrom, 2019. Factors influencing aquatic and terrestrial bacterial community assembly. Environmental Microbiology Reports 11: 306–315.

    PubMed  Google Scholar 

  • Langille, M. G. I., J. Zaneveld, J. G. Caporaso, D. McDonald, D. Knights, J. A. Reyes, J. C. Clemente, D. E. Burkepile, R. L. Vega Thurber, R. Knight, R. G. Beiko & C. Huttenhower, 2013. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nature Biotechnology 31: 814–821.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Leake, J. R. & D. J. Read, 1990. Chitin as a nitrogen source for mycorrhizal fungi. Mycological Research 94: 993–995.

    CAS  Google Scholar 

  • Lehnen, N., H. K. Marchant, A. Schwedt, J. Milucka, C. Lott, M. Weber, J. Dekaezemacker, B. K. B. Seah, P. F. Hach, W. Mohr & M. M. M. Kuypers, 2016. High rates of microbial dinitrogen fixation and sulfate reduction associated with the Mediterranean seagrass Posidonia oceanica. Systematic and Applied Microbiology 39: 476–483.

    CAS  PubMed  Google Scholar 

  • Leininger, S., T. Urich, M. Schloter, L. Schwark, J. Qi, G. W. Nicol, J. I. Prosser, S. C. Schuster & C. Schleper, 2006. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442: 806–809.

    ADS  CAS  PubMed  Google Scholar 

  • Mathai, P. P., H. M. Dunn, P. Magnone, Q. Zhang, S. Ishii, C. L. Chun & M. J. Sadowsky, 2019. Association between submerged aquatic vegetation and elevated levels of Escherichia coli and potential bacterial pathogens in freshwater lakes. Science of the Total Environment 657: 319–324.

    ADS  CAS  PubMed  Google Scholar 

  • McMurdie, P. J. & S. Holmes, 2012. Phyloseq: A bioconductor package for handling and analysis of high-throughput phylogenetic sequence data. In Altman, R. B., A. K. Dunker, L. Hunter & T. A. Murray (eds), Pacific Symposium on Biocomputing 2012 World Scientific, London: 235–246.

    Google Scholar 

  • Moliné, M., M. R. Flores, D. Libkind, M. Del Carmen Diéguez, M. E. Farías & M. Van Broock, 2010. Photoprotection by carotenoid pigments in the yeast Rhodotorula mucilaginosa: The role of torularhodin. Photochemical and Photobiological Sciences 9: 1145–1151.

    PubMed  Google Scholar 

  • Murphy, J. & J. P. Riley, 1962. A modified single solution method for the determination of phosphate in natural waters. Analytica Chimica Acta 27: 31–36.

    CAS  Google Scholar 

  • Nilsson, R. H., K. H. Larsson, A. F. S. Taylor, J. Bengtsson-Palme, T. S. Jeppesen, D. Schigel, P. Kennedy, K. Picard, F. O. Glöckner, L. Tedersoo, I. Saar, U. Kõljalg & K. Abarenkov, 2019. The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Research 47: D259–D264.

    CAS  PubMed  Google Scholar 

  • O’Brien, A. M., Z. H. Yu, D. ya Luo, J. Laurich, E. Passeport & M. E. Frederickson, 2020. Resilience to multiple stressors in an aquatic plant and its microbiome. American Journal of Botany 107: 273–285.

    PubMed  Google Scholar 

  • Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P. R., O'Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H. H., Szoecs, E. & H. Wagner, 2020. vegan: Community Ecology Package. R package version 2.5-7. https://CRAN.R-project.org/package=vegan

  • Paula, C. C. P., P. Macek, J. Bárta, J. Borovec, I. Svobodová, E. Holá, J. Lepš & D. Sirová, 2022. Parasitic trophic mode of plant host affects the extent of colonization, but does not induce systematic shifts in the composition of foliar endophytic assemblages in temperate meadow ecosystems. Functional Ecology 36: 1177–1190.

    Google Scholar 

  • Pettit, N. E., D. P. Ward, M. F. Adame, D. Valdez & S. E. Bunn, 2016. Influence of aquatic plant architecture on epiphyte biomass on a tropical river floodplain. Aquatic Botany 129: 35–43.

    Google Scholar 

  • Prendergast-Miller, M. T., E. M. Baggs & D. Johnson, 2011. Nitrous oxide production by the ectomycorrhizal fungi Paxillus involutus and Tylospora fibrillosa. FEMS Microbiology Letters 316: 31–35.

    CAS  PubMed  Google Scholar 

  • Quast, C., E. Pruesse, P. Yilmaz, J. Gerken, T. Schweer, P. Yarza, J. Peplies & F. O. Glöckner, 2013. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research 41: D590–D596.

    CAS  PubMed  Google Scholar 

  • Rabemanolontsoa, H. & S. Saka, 2012. Characterization of Lake Biwa macrophytes in their chemical composition. Journal of the Japan Institute of Energy 91: 621–628.

    CAS  Google Scholar 

  • Rao, S., J. Reiskind & G. Bowes, 2006. Light regulation of the photosynthetic phosphoenolpyruvate carboxylase (PEPC) in Hydrilla verticillata. Plant and Cell Physiology 47: 1206–1216.

    CAS  PubMed  Google Scholar 

  • Rashmi, M., J. S. Kushveer & V. V. Sarma, 2019. A worldwide list of endophytic fungi with notes on ecology and diversity. Mycosphere 10: 798–1079.

    Google Scholar 

  • Redford, A. J., R. M. Bowers, R. Knight, Y. Linhart & N. Fierer, 2010. The ecology of the phyllosphere: geographic and phylogenetic variability in the distribution of bacteria on tree leaves. Environmental Microbiology 12: 2885–2893.

    PubMed  PubMed Central  Google Scholar 

  • Reguera, G. & S. B. Leschine, 2001. Chitin degradation by cellulolytic anaerobes and facultative aerobes from soils and sediments. FEMS Microbiology Letters 204: 367–374.

    CAS  PubMed  Google Scholar 

  • Reitsema, R. E., P. Meire & J. Schoelynck, 2018. The future of freshwater macrophytes in a changing world: dissolved organic carbon quantity and quality and its interactions with macrophytes. Frontiers in Plant Science 9: 629.

    PubMed  PubMed Central  Google Scholar 

  • Rejmánková, E., D. Sirová, S. T. Castle, J. Bárta & H. Carpenter, 2018a. Heterotrophic N2-fixation contributes to nitrogen economy of a common wetland sedge Schoenoplectus californicus. PLoS ONE 13: e0195570.

    PubMed  PubMed Central  Google Scholar 

  • Rejmánková, E., B. W. Sullivan, J. R. Ortiz Aldana, J. M. Snyder, S. T. Castle & F. Reyes Morales, 2018b. Regime shift in the littoral ecosystem of volcanic Lake Atitlán in Central America: combined role of stochastic event and invasive plant species. Freshwater Biology 63: 1088–1106.

    Google Scholar 

  • Reyes Morales, F., D. Ujpan & S. Valiente, 2018. Bathymetry and morphometric analysis of Atitlán Lake. Revista Científica 27: 48–58.

    Google Scholar 

  • Segata, N., J. Izard, L. Waldron, D. Gevers, L. Miropolsky, W. S. Garrett & C. Huttenhower, 2011. Metagenomic biomarker discovery and explanation. Genome Biology 12: 1–18.

    Google Scholar 

  • Selosse, M.-A. & C. Strullu-Derrien, 2015. Origins of the terrestrial flora: a symbiosis with fungi? BIO Web of Conferences 4: 9.

    Google Scholar 

  • Singh, R. S., G. K. Saini & J. F. Kennedy, 2008. Pullulan: microbial sources, production and applications. Carbohydrate Polymers 73: 515–531.

    CAS  PubMed  Google Scholar 

  • Sirová, D., J. Šantrůček, L. Adamec, J. Bárta, J. Borovec, J. Pech, S. M. Owens, H. Šantrůčková, R. Schäufele, H. Štorchová & J. Vrba, 2014. Dinitrogen fixation associated with shoots of aquatic carnivorous plants: is it ecologically important? Annals of Botany 114: 125–133.

    PubMed  PubMed Central  Google Scholar 

  • Søndergaard, M., G. Phillips, S. Helsten, A. Kolada, F. Ecke, H. Maemets, M. Mjelde, M. Azzella & A. Oggioni, 2013. Maximum growing depth of submerged macrophytes in European lakes. Hydrobiologia 704: 165–177.

    Google Scholar 

  • Sousa, W. T. Z., 2011. Hydrilla verticillata (Hydrocharitaceae), a recent invader threatening Brazil’s freshwater environments: a review of the extent of the problem. Hydrobiologia 669: 1–20.

    Google Scholar 

  • Srivastava, J. K., H. Chandra, S. J. S. Kalra, P. Mishra, H. Khan & P. Yadav, 2017. Plant–microbe interaction in aquatic system and their role in the management of water quality: a review. Applied Water Science 7: 1079–1090.

    ADS  CAS  Google Scholar 

  • Strayer, D. L. & S. E. G. Findlay, 2010. Ecology of freshwater shore zones. Aquatic Sciences 72: 127–163.

    CAS  Google Scholar 

  • Strullu-Derrien, C., M. A. Selosse, P. Kenrick & F. M. Martin, 2018. The origin and evolution of mycorrhizal symbioses: from palaeomycology to phylogenomics. New Phytologist 220: 1012–1030.

    PubMed  Google Scholar 

  • Su, X., G. Jing, Y. Zhang & S. Wu, 2020. Method development for cross-study microbiome data mining: challenges and opportunities. Computational and Structural Biotechnology Journal 18: 2075–2080.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tedersoo, L., M. Bahram, S. Põlme, U. Kõljalg, N. S. Yorou, R. Wijesundera, L. V. Ruiz, A. M. Vasco-Palacios, P. Q. Thu, A. Suija, M. E. Smith, C. Sharp, E. Saluveer, A. Saitta, M. Rosas, T. Riit, D. Ratkowsky, K. Pritsch, K. Põldmaa, M. Piepenbring, C. Phosri, M. Peterson, K. Parts, K. Pärtel, E. Otsing, E. Nouhra, A. L. Njouonkou, R. H. Nilsson, L. N. Morgado, J. Mayor, T. W. May, L. Majuakim, D. J. Lodge, S. Lee, K. H. Larsson, P. Kohout, K. Hosaka, I. Hiiesalu, T. W. Henkel, H. Harend, L. D. Guo, A. Greslebin, G. Grelet, J. Geml, G. Gates, W. Dunstan, C. Dunk, R. Drenkhan, J. Dearnaley, A. De Kesel, T. Dang, X. Chen, F. Buegger, F. Q. Brearley, G. Bonito, S. Anslan, S. Abell & K. Abarenkov, 2014. Global diversity and geography of soil fungi. Science American Association for the Advancement of Science. https://doi.org/10.1126/science.1256688.

    Article  Google Scholar 

  • Thompson, L., J. Sanders, D. McDonald, A. Amir, J. Ladau, K. J. Locey, R. J. Prill, A. Tripathi, S. M. Gibbons, G. Ackerman, J. A. Navas-Molina, S. Janssen, E. Kopylova, Y. Vázquez-Baeza, A. Gonzáles, J. T. Morton, S. Mirarab, Z. Z. Xu, L. Jiang, M. F. Haroon, J. Kanbar, Q. Zhu, S. J. Song, T. Kosciolek, N. A. Bokulich, J. Lefler, C. J. Brislawn, G. Humphrey, S. M. Owens, J. Hampton-Marcell, D. Berg-Lyons, V. McKenzie, N. Fierer, J. A. Fuhrman, A. Clauset, R. L. Stevens, A. Shade, K. S. Pollard, K. D. Goodwin, J. K. Jansson, J. A. Gilbert, R. Knight, The Earth Microbiome Project Consortium, 2017. A communal catalogue reveals Earth’s multiscale microbial diversity. Nature 551: 457–463.

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, B. & S. Sugiyama, 2020. Phylogenetic signal of host plants in the bacterial and fungal root microbiomes of cultivated angiosperms. Plant Journal 104: 522–531.

    CAS  Google Scholar 

  • Wei, X., J. Chen, C. Zhang & D. Pan, 2016. A new Oidiodendron maius strain isolated from Rhododendron fortunei and its effects on nitrogen uptake and plant growth. Frontiers in Microbiology 7: 1327.

    PubMed  PubMed Central  Google Scholar 

  • Wetzel, R. G. & M. Søndergaard, 1998. Role of submerged macrophytes for the microbial community and dynamics of dissolved organic carbon in aquatic ecosystems. In Jeppesen, E., M. Søndergaard, M. Søndergaard & K. Christoffersen (eds), The Structuring Role of Submerged Macrophytes in Lakes Springer, New York: 133–148.

    Google Scholar 

  • Wisnoski, N. I., M. E. Muscarella, M. L. Larsen, A. L. Peralta & J. T. Lennon, 2020. Metabolic insight into bacterial community assembly across ecosystem boundaries. Ecology Ecological Society of America 101: e02968.

    Google Scholar 

  • Wolfe, E. R., B. S. Younginger & C. J. LeRoy, 2019. Fungal endophyte-infected leaf litter alters in-stream microbial communities and negatively influences aquatic fungal sporulation. Oikos 128: 405–415.

    ADS  Google Scholar 

  • Xiong, J., Y. Liu, X. Lin, H. Zhang, J. Zeng, J. Hou, Y. Yang, T. Yao, R. Knight & H. Chu, 2012. Geographic distance and pH drive bacterial distribution in alkaline lake sediments across Tibetan Plateau. Environmental Microbiology 14: 2457–2466.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zanchetta, E., E. Damergi, B. Patel, T. Borgmeyer, H. Pick, A. Pulgarin & C. Ludwig, 2021. Algal cellulose, production and potential use in plastics: challenges and opportunities. Algal Research 56: 102288.

    Google Scholar 

  • Zarraonaindia, I., S. M. Owens, P. Weisenhorn, K. West, J. Hampton-Marcell, S. Lax, N. A. Bokulich, D. A. Mills, G. Martin, S. Taghavi, D. van der Lelie & J. A. Gilbert, 2015. The soil microbiome influences grapevine-associated microbiota. Mbio 6: e02527-e2614.

    PubMed  PubMed Central  Google Scholar 

  • Zuberer, D. A., 1982. Nitrogen fixation (acetylene reduction) associated with duckweed (Lemnaceae) mats. Applied and Environmental Microbiology 43: 823–828.

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Zulkifly, S., A. Hanshew, E. B. Young, P. Lee, M. E. Graham, M. Piotrowski & L. E. Graham, 2012. The epiphytic microbiota of the globally widespread macroalga Cladophora glomerata (Chlorophyta, Cladophorales). American Journal of Botany 99: 1541–1552.

    PubMed  Google Scholar 

  • Zulkifly, S. B., J. M. Graham, E. B. Young, R. J. Mayer, M. J. Piotrowski, I. Smith & L. E. Graham, 2013. The Genus Cladophora Kützing (Ulvophyceae) as a Globally Distributed Ecological Engineer. Journal of Phycology 49: 1–17.

    PubMed  Google Scholar 

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Acknowledgements

The study was supported by the Grant Agency of the Czech Republic Project No. P504/17-10493S, and UC Davis Academic Senate grant. We thank the Asociación de Amigos del Lago de Atitlan, CEA–UVG Altiplano, and AMSCLAE for logistical and personnel support. We would also like to thank Martina Čtvrtlíková and Lubomír Adamec for their valuable comments during the manuscript writing period.

Funding

Funding was provided by Grantová Agentura České Republiky (Grant No. P504/17-10493S), UC Davis College of Biological Sciences.

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Authors and Affiliations

  1. Institute of Hydrobiology, Biology Centre CAS, Na Sádkách 7, 37005, Ceske Budejovice, Czech Republic

    Caio Cesar Pires de Paula, Jiří Bárta, Jaroslava Komárková, Qiang Lin, Iva Kohoutová & Dagmara Sirová

  2. Faculty of Science, University of South Bohemia, Branišovská 1760, 37005, Ceske Budejovice, Czech Republic

    Jiří Bárta

  3. Department of Environmental Science and Policy, University of California, One Shields Avenue, Davis, CA, 95616, USA

    Eliška Rejmánková

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  1. Caio Cesar Pires de Paula
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  2. Jiří Bárta
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Correspondence to Dagmara Sirová.

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“In memory of Brij Gopal, one of the founding fathers of wetland ecology”.

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Supplementary Information

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Supplementary file1 (PDF 108 KB)

Figure S1. Guatemala location overview and highlight for Lake Atitlán, Guatemala, CA, with sampling locations (stars) near the San Juan (A), Santiago (B), and San Lucas (C) settlements (modified map from Emery & Brown, 2012).

Supplementary file2 (PDF 392 KB)

Figure S2. Proportion of functional genes involved in organic matter degradation in Hydrilla (Hyd) and Cladophora (Cld) microbiomes. The relative abundances of detected taxa are shown in blue (a). Green plots (b) show the percentage (out of the total number of OTUs) of taxa with confirmed presence of the respective functional gene in the genome.

Supplementary file3 (XLSX 1380 KB)

Table S1. Operational Taxonomic Unit (OTU) table listing all bacterial and fungal OTUs identified in the study.

Supplementary file4 (DOCX 15 KB)

Table S2. List of algal and cyanobacterial species/genera identified in the samples by microscopy, and their presence at the three distinct sampling locations.

Supplementary file5 (XLSX 65 KB)

Table S3. Functional predictions for bacterial taxa (FunGene database output)

Supplementary file6 (XLSX 23 KB)

Table S4. Co-occurrence analysis results listing important network parameters

Supplementary file7 (XLSX 10 KB)

Table S5. Mapping file containing relevant metadata

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de Paula, C.C.P., Bárta, J., Rejmánková, E. et al. The role of macrophyte-associated microbiomes in lacustrine wetlands: an example of the littoral zone of lake Atitlan, Guatemala. Hydrobiologia 851, 1637–1655 (2024). https://doi.org/10.1007/s10750-022-05043-z

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