Hunters or farmers? Microbiome characteristics help elucidate the diet composition in an aquatic carnivorous plant
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
30558682
PubMed Central
PMC6297986
DOI
10.1186/s40168-018-0600-7
PII: 10.1186/s40168-018-0600-7
Knihovny.cz E-zdroje
- Klíčová slova
- Algae, Bacteria, Ciliate bacterivory, Digestive mutualism, Fungi, Herbivory, Nutrient turnover, Plant–microbe interactions, Protists, Utricularia traps,
- MeSH
- Bacteria klasifikace genetika izolace a purifikace MeSH
- DNA bakterií genetika MeSH
- DNA fungální genetika MeSH
- DNA řas genetika MeSH
- fylogeneze MeSH
- hluchavkotvaré mikrobiologie fyziologie MeSH
- houby klasifikace genetika izolace a purifikace MeSH
- metagenomika metody MeSH
- mikrobiální společenstva MeSH
- stanovení celkové genové exprese metody MeSH
- vodní organismy mikrobiologie fyziologie MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- DNA bakterií MeSH
- DNA fungální MeSH
- DNA řas MeSH
BACKGROUND: Utricularia are rootless aquatic carnivorous plants which have recently attracted the attention of researchers due to the peculiarities of their miniaturized genomes. Here, we focus on a novel aspect of Utricularia ecophysiology-the interactions with and within the complex communities of microorganisms colonizing their traps and external surfaces. RESULTS: Bacteria, fungi, algae, and protozoa inhabit the miniature ecosystem of the Utricularia trap lumen and are involved in the regeneration of nutrients from complex organic matter. By combining molecular methods, microscopy, and other approaches to assess the trap-associated microbial community structure, diversity, function, as well as the nutrient turn-over potential of bacterivory, we gained insight into the nutrient acquisition strategies of the Utricularia hosts. CONCLUSIONS: We conclude that Utricularia traps can, in terms of their ecophysiological function, be compared to microbial cultivators or farms, which center around complex microbial consortia acting synergistically to convert complex organic matter, often of algal origin, into a source of utilizable nutrients for the plants.
Biology Centre CAS Institute of Hydrobiology Na Sádkách 7 CZ 37005 České Budějovice Czech Republic
Department of Biology and Wildlife University of Alaska Fairbanks Fairbanks AK 99775 USA
Institute of Botany CAS Dukelská 135 CZ 37982 Třeboň Czech Republic
Institute of Experimental Botany CAS Rozvojová 263 CZ 16502 Praha 6 Lysolaje Czech Republic
Zobrazit více v PubMed
Berg G, Grube M, Schloter M, Smalla K. Unraveling the plant microbiome: looking back and future perspectives. Front Microbiol. 2014;5:148. PubMed PMC
Rinke C, Schwientek P, Sczyrba A, Ivanova NN, Anderson IJ, Cheng J-F, et al. Insights into the phylogeny and coding potential of microbial dark matter. Nature. 2013;499:431–437. doi: 10.1038/nature12352. PubMed DOI
Sirová D, Borovec J, Černá B, Rejmánková E, Adamec L, Vrba J. Microbial community development in the traps of aquatic Utricularia species. Aquat Bot. 2009;90:129–136. doi: 10.1016/j.aquabot.2008.07.007. DOI
Caravieri FA, Ferreira AJ, Ferreira A, Clivati D, de Miranda VFO, Araújo WL. Bacterial community associated with traps of the carnivorous plants Utricularia hydrocarpa and Genlisea filiformis. Aquat Bot. 2014;116:8–12. doi: 10.1016/j.aquabot.2013.12.008. DOI
Alcaraz LD, Martínez-Sánchez S, Torres I, Ibarra-Laclette E, Herrera-Estrella L. The metagenome of Utricularia gibba’s traps: into the microbial input to a carnivorous plant. PLoS One. 2016;11:e0148979. doi: 10.1371/journal.pone.0148979. PubMed DOI PMC
Díaz-Olarte J, Valoyes-Valois V, Guisande C, Torres NN, González-Bermúdez A, Sanabria-Aranda L, et al. Periphyton and phytoplankton associated with the tropical carnivorous plant Utricularia foliosa. Aquat Bot. 2007;87:285–291. doi: 10.1016/j.aquabot.2007.06.010. DOI
Sirová D, Borovec J, Šantrůčková H, Šantrůček J, Vrba J, Adamec L. Utricularia carnivory revisited: plants supply photosynthetic carbon to traps. J Exp Bot. 2010;61:99–103. doi: 10.1093/jxb/erp286. PubMed DOI
Sirová D, Borovec J, Picek T, Adamec L, Nedbalová L, Vrba J. Ecological implications of organic carbon dynamics in the traps of aquatic carnivorous Utricularia plants. Funct Plant Biol. 2011;38:583–593. doi: 10.1071/FP11023. PubMed DOI
Carretero-Paulet L, Chang TH, Librado P, Ibarra-Laclette E, Herrera-Estrella L, Rozas J, et al. Genome-wide analysis of adaptive molecular evolution in the carnivorous plant Utricularia gibba. Genome Biol Evol. 2015;7:444–456. doi: 10.1093/gbe/evu288. PubMed DOI PMC
Carretero-Paulet L, Librado P, Chang TH, Ibarra-Laclette E, Herrera-Estrella L, Rozas J, et al. High gene family turnover rates and gene space adaptation in the compact genome of the carnivorous plant Utricularia gibba. Mol Biol Evol. 2015;32:1284–1295. doi: 10.1093/molbev/msv020. PubMed DOI
Silva SR, Alvarenga DO, Aranguren Y, Penha HA, Fernandes CC, Pinheiro DG, et al. The mitochondrial genome of the terrestrial carnivorous plant Utricularia reniformis (Lentibulariaceae): structure, comparative analysis and evolutionary landmarks. PLoS One. 2017;12:e0180484. doi: 10.1371/journal.pone.0180484. PubMed DOI PMC
Adamec L. Oxygen concentrations inside the traps of the carnivorous plants Utricularia and Genlisea (Lentibulariaceae) Ann Bot. 2007;100:849–856. doi: 10.1093/aob/mcm182. PubMed DOI PMC
Sirová D, Bárta J, Borovec J, Vrba J. The Utricularia-associated microbiome: composition, function, and ecology. Carnivorous Plants Physiology, Ecology, and Evolution. Oxford University Press. 2018;Chapter 25: 349–58.
Darwin C. Insectivorous plants. New York: D. Appleton and Company; 1875.
Richards JH. Bladder function in Utricularia purpurea (Lentibulariaceae): is carnivory important? Am J Bot. 2001;88:170–6. PubMed
Friday LE. Rapid turnover of traps in Utricularia vulgaris L. Oecologia. 1989;80:272–277. doi: 10.1007/BF00380163. PubMed DOI
Płachno BJ, Łukaszek M, Wołowski K, Adamec L, Stolarczyk P. Aging of Utricularia traps and variability of microorganisms associated with that microhabitat. Aquat Bot. 2012;97:44–47. doi: 10.1016/j.aquabot.2011.11.003. DOI
Peroutka M, Adlassnig W, Volgger M, Lendl T, Url WG, Lichtscheidl IK. Utricularia: a vegetarian carnivorous plant? Agae as prey of bladderwort in oligotrophic bogs. Plant Ecol. 2008;199:153–162. doi: 10.1007/s11258-008-9420-3. DOI
Alkhalaf IA, Hübener T, Porembski S. Prey spectra of aquatic Utricularia species (Lentibulariaceae) in northeastern Germany: the role of planktonic algae. Flora Morphol Distrib Funct Ecol Plants. 2009;204:700–708. doi: 10.1016/j.flora.2008.09.008. DOI
Nalepa C a, Bignell DE, Bandi C. Detritivory, coprophagy, and the evolution of digestive mutualisms in Dictyoptera. Insect Soc. 2001;48:194–201. doi: 10.1007/PL00001767. DOI
Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, et al. Evolution of mammals and their gut microbes. Science. 2008;320:1647–1651. doi: 10.1126/science.1155725. PubMed DOI PMC
Barboza PS, Bennett A, Lignot J-H, Mackie RI, McWhorter TJ, Secor SM, et al. Digestive challenges for vertebrate animals: microbial diversity, cardiorespiratory coupling, and dietary specialization. Physiol Biochem Zool. 2010;83:764–774. doi: 10.1086/650472. PubMed DOI
Adamec L. Functional characteristics of traps of aquatic carnivorous Utricularia species. Aquat Bot. 2011;3:226–233. doi: 10.1016/j.aquabot.2011.07.001. PubMed DOI
Adlassnig W, Peroutka M, Lendl T. Traps of carnivorous pitcher plants as a habitat: composition of the fluid, biodiversity and mutualistic activities. Ann Bot. 2011;107:181–194. doi: 10.1093/aob/mcq238. PubMed DOI PMC
Troyer K. Diet selection and digestion in Iguana iguana: the importance of age and nutrient requirements. Oecologia. 1984;61:201–207. doi: 10.1007/BF00396761. PubMed DOI
Berg M, Zhou XY, Shapira M. Host-specific functional significance of Caenorhabditis gut commensals. Front Microbiol. 2016. 10.3389/fmicb.2016.01622. PubMed PMC
Willems A. The family Comamonadaceae. The prokaryotes: alphaproteobacteria and Betaproteobacteria. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F, editors. The Prokaryotes. Berlin: Springer; 2014.
Slobodkin A. The family peptostreptococcaceae. The prokaryotes: firmicutes and tenericutes. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F, editors. The Prokaryotes. Berlin: Springer; 2014.
Attwood GT, Klieve AV, Ouwerkerk D, Patel BKC. Ammonia-hyperproducing bacteria from New Zealand ruminants. Appl Environ Microbiol. 1998;64:1796–1804. PubMed PMC
Sirová D, Šantrůček J, Adamec L, Bárta J, Borovec J, Pech J, et al. Dinitrogen fixation associated with shoots of aquatic carnivorous plants: is it ecologically important? Ann Bot. 2014;114:125–133. doi: 10.1093/aob/mcu067. PubMed DOI PMC
Velicer GJ, Mendes-Soares H. Bacterial predators. Curr Biol. 2009;19:R55–R56. doi: 10.1016/j.cub.2008.10.043. PubMed DOI
Chauhan A, Cherrier J, Williams HN. Impact of sideways and bottom-up control factors on bacterial community succession over a tidal cycle. PNAS. 2009;106:4301–4306. doi: 10.1073/pnas.0809671106. PubMed DOI PMC
Dawid W. Biology and global distribution of myxobacteria in soils. FEMS Microbiol Rev. 2000;24:403–427. doi: 10.1111/j.1574-6976.2000.tb00548.x. PubMed DOI
Popper ZA, Michel G, Hervé C, Domozych DS, Willats WGT, Tuohy MG, et al. Evolution and diversity of plant cell walls: from algae to flowering plants. Annu Rev Plant Biol. 2011;62:567–590. doi: 10.1146/annurev-arplant-042110-103809. PubMed DOI
Yapi Assoi Yapi D, Gnakri D, Lamine Niamke S, Patrice Kouame L. Purification and biochemical characterization of a specific beta-glucosidase from the digestive fluid of larvae of the palm weevil, Rhynchophorus palmarum. J Insect Sci. 2009;9:4. doi: 10.1673/031.009.0401. PubMed DOI PMC
Chen B, Teh BS, Sun C, Hu S, Lu X, Boland W, et al. Biodiversity and activity of the gut microbiota across the life history of the insect herbivore Spodoptera littoralis. Sci Rep. 2016;6:29505. doi: 10.1038/srep29505. PubMed DOI PMC
Petit C, Rigg GP, Pazzani C, Smith A, Sieberth V, Stevens M, et al. Region 2 of the Escherichia coli K5 capsule gene cluster encoding proteins for the biosynthesis of the K5 polysaccharide. Mol Microbiol. 1995;17:611–620. doi: 10.1111/j.1365-2958.1995.mmi_17040611.x. PubMed DOI
González-Rodríguez I, Sánchez B, Ruiz L, Turroni F, Ventura M, Ruas-Madiedo P, et al. Role of extracellular transaldolase from Bifidobacterium bifidum in mucin adhesion and aggregation. Appl Environ Microbiol. 2012;78:3992–3998. doi: 10.1128/AEM.08024-11. PubMed DOI PMC
Hackstein JHP, Van Alen TA. Fecal methanogens and vertebrate evolution. Evolution. 2016;50:559–572. doi: 10.1111/j.1558-5646.1996.tb03868.x. PubMed DOI
Repeta DJ, Ferrón S, Sosa OA, Johnson CG, Repeta LD, Acker M, et al. Marine methane paradox explained by bacterial degradation of dissolved organic matter. Nat Geosci. 2016;9:884–887. doi: 10.1038/ngeo2837. DOI
Towne G, Nagaraja TG, Brandt RT, Kemp KE. Dynamics of ruminal ciliated protozoa in feedlot cattle. Appl Environ Microbiol. 1990;56:3174–3178. PubMed PMC
Abraham JV, Butler RD, Sigee DC. Ciliate populations and metals in an activated-sludge plant. Water Res. 1997;31:1103–1111. doi: 10.1016/S0043-1354(96)00334-X. DOI
Pitsch G, Adamec L, Dirren S, Nitsche F, Šimek K, Sirová D, et al. The green Tetrahymena utriculariae n. sp. (Ciliophora, Oligohymenophorea) with its endosymbiotic algae (Micractinium sp.), living in traps of a carnivorous aquatic plant. J Eukaryot Microbiol. 2017;64:322–335. doi: 10.1111/jeu.12369. PubMed DOI
Šimek K, Pitsch G, Salcher MM, Sirová D, Shabarova T, Adamec L, et al. Ecological traits of the algae-bearing Tetrahymena utriculariae (Ciliophora) from traps of the aquatic carnivorous plant Utricularia reflexa. J Eukaryot Microbiol. 2017;64:336–348. doi: 10.1111/jeu.12368. PubMed DOI
Šimek K, Jürgens K, Nedoma J, Comerma M, Armengol J. Ecological role and bacterial grazing of Halteria spp.: small freshwater oligotrichs as dominant pelagic ciliate bacterivores. Aquat Microb Ecol. 2000;22:43–56. doi: 10.3354/ame022043. DOI
Simek K, Armengol J, Comerma M, Garcia JC, Chrzanowski TH, Macek M, et al. Characteristics of protistan control of bacterial production in three reservoirs of different trophy. Int Rev Hydrobiol. 1998;83:485–494. doi: 10.1002/iroh.19980830103. DOI
Thouvenot A. Bacterivory of metazooplankton, ciliates and flagellates in a newly flooded reservoir. J Plankton Res. 1999;21:1659–1679. doi: 10.1093/plankt/21.9.1659. DOI
Laybourn-Parry J. Protozoan plankton ecology. London: Chapman and Hall; 1992.
Neuer S, Cowles TJ. Comparative size-specific grazing rates in field populations of ciliates and dinoflagellates. Mar Ecol Prog Ser. 1995;61:99–103.
Koeck DE, Pechtl A, Zerlov VV, et al. Genomics of cellulolytic bacteria. Curr Opin Biotech. 2014;29:171–83. PubMed
Adamec L, Sirová D, Vrba J. Contrasting growth effects of prey capture in two aquatic carnivorous plant species. Fundam Appl Limnol / Arch für Hydrobiol. 2010;176:153–160. doi: 10.1127/1863-9135/2010/0176-0153. DOI
Borovec J, Sirová D, Adamec L. Light as a factor affecting the concentration of simple organics in the traps of aquatic carnivorous Utricularia species. Fundam Appl Limnol / Arch für Hydrobiol. 2012;181:159–166. doi: 10.1127/1863-9135/2012/0271. DOI
Urich T, Lanzen A, Qi J, Huson DH, Schleper C, Schuster SC. Simultaneous assessment of soil microbial community structure and function through analysis of the meta-transcriptome. PLoS One. 2008;3:e2527. doi: 10.1371/journal.pone.0002527. PubMed DOI PMC
Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, et al. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature. 2006;442:806–809. doi: 10.1038/nature04983. PubMed DOI
Liu Z, Lozupone C, Hamady M, Bushman FD, Knight R. Short pyrosequencing reads suffice for accurate microbial community analysis. Nucleic Acids Res. 2007;35:e120. doi: 10.1093/nar/gkm541. PubMed DOI PMC
Bates ST, Berg-Lyons D, Caporaso JG, Walters WA, Knight R, Fierer N. Examining the global distribution of dominant archaeal populations in soil. ISME J. 2011;5:908–917. doi: 10.1038/ismej.2010.171. PubMed DOI PMC
Bergmann GT, Bates ST, Eilers KG, Lauber CL, Caporaso JG, Walters WA, et al. The under-recognized dominance of Verrucomicrobia in soil bacterial communities. Soil Biol Biochem. 2011;43:1450–1455. doi: 10.1016/j.soilbio.2011.03.012. PubMed DOI PMC
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–336. doi: 10.1038/nmeth.f.303. PubMed DOI PMC
Segata N, Izard J, Walron L, Gevers D, Miropolsky L, Garrett W, Huttenhower C. Metagenomic biomarker discovery and explanation. Gen Biol. 2011;12:R60. doi: 10.1186/gb-2011-12-6-r60. PubMed DOI PMC
Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 2008;15:78. PubMed PMC
Bárta J, Stone JD, Pech J, Sirová D, Adamec L, Campbell MA, et al. The transcriptome of Utricularia vulgaris, a rootless plant with minimalist genome, reveals extreme alternative splicing and only moderate sequence similarity with Utricularia gibba. BMC Plant Biol. 2015;15:78. doi: 10.1186/s12870-015-0467-8. PubMed DOI PMC
Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc. 2013;8:1494–1512. doi: 10.1038/nprot.2013.084. PubMed DOI PMC
Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nat Methods. 2015;12:59–60. doi: 10.1038/nmeth.3176. PubMed DOI
Huson DH, Beier S, Flade I, Górska A, El-Hadidi M, Mitra S, et al. MEGAN Community Edition - interactive exploration and analysis of large-scale microbiome sequencing data. PLoS Comput Biol. 2016;12:e1004957. doi: 10.1371/journal.pcbi.1004957. PubMed DOI PMC
Fish JA, Chai B, Wang Q, Sun Y, Brown CT, Tiedje JM, et al. FunGene: the functional gene pipeline and repository. Front Microbiol. 2013;4:291. PubMed PMC
Berry D, Widder S. Deciphering microbial interactions and detecting keystone species with co-occurrence networks. Front Microbiol. 2014;5:219. doi: 10.3389/fmicb.2014.00219. PubMed DOI PMC
Weiss S, Van Treuren W, Lozupone C, Faust K, Friedman J, Deng Y, et al. Correlation detection strategies in microbial data sets vary widely in sensitivity and precision. ISME J. 2016;10:1669–1681. doi: 10.1038/ismej.2015.235. PubMed DOI PMC
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13:2498–2504. doi: 10.1101/gr.1239303. PubMed DOI PMC
Faust K, Sathirapongsasuti JF, Izard J, Segata N, Gevers D, Raes J, et al. Microbial co-occurrence relationships in the human microbiome. PLoS Comput Biol. 2012;8:e1002606. PubMed PMC
Recent ecophysiological, biochemical and evolutional insights into plant carnivory