Mutualistic Outcomes Across Plant Populations, Microbes, and Environments in the Duckweed Lemna minor

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Abstract

The picture emerging from the rapidly growing literature on host-associated microbiota is that host traits and fitness often depend on interactive effects of host genotype, microbiota, and abiotic environment. However, testing interactive effects typically requires large, multi-factorial experiments and thus remains challenging in many systems. Furthermore, most studies of plant microbiomes focus on terrestrial hosts and microbes. Aquatic habitats may confer unique properties to microbiomes. We grew different populations of duckweed (Lemna minor), a floating aquatic plant, in three microbial treatments (adding no, “home”, or “away” microbes) at two levels of zinc, a common water contaminant in urban areas, and measured both plant and microbial performance. Thus, we simultaneously manipulated plant source population, microbial community, and abiotic environment. We found strong effects of plant source, microbial treatment, and zinc on duckweed and microbial growth, with significant variation among duckweed genotypes and microbial communities. However, we found little evidence of interactive effects: zinc did not alter effects of host genotype or microbial community, and host genotype did not alter effects of microbial communities. Despite strong positive correlations between duckweed and microbe growth, zinc consistently decreased plant growth, but increased microbial growth. Furthermore, as in recent studies of terrestrial plants, microbial interactions altered a duckweed phenotype (frond aggregation). Our results suggest that duckweed source population, associated microbiome, and contaminant environment should all be considered for duckweed applications, such as phytoremediation. Lastly, we propose that duckweed microbes offer a robust experimental system for study of host–microbiota interactions under a range of environmental stresses.

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References

  1. 1.

    Clausen J, Keck DD, Hiesey WM (1947) Heredity of geographically and ecologically isolated races. Am Nat 81(797):114– 133

    PubMed  CAS  Google Scholar 

  2. 2.

    Rehfeldt GE, Tchebakova NM, Parfenova YI, Wykoff WR, Kuzmina NA, Milyutin LI (2002) Intraspecific responses to climate in Pinus Sylvestris. Global Change Biol 8(9):912–929. https://doi.org/10.1046/j.1365-2486.2002.00516.x. ISSN 1365-2486

    Article  Google Scholar 

  3. 3.

    Wilczek AM, Cooper MD, Korves TM, Schmitt J (2014) Lagging adaptation to warming climate in Arabidopsis Thaliana. Proc Natl Acad Sci 111(22):7906–7913. https://doi.org/10.1073/pnas.1406314111

    Article  PubMed  CAS  Google Scholar 

  4. 4.

    Zhu X-C, Song F-B, Xu H-W (2009) Arbuscular mycorrhizae improves low temperature stress in maize via alterations in host water status and photosynthesis. Plant Soil 331 (1–2):129–137. https://doi.org/10.1007/s11104-009-0239-z

    Article  CAS  Google Scholar 

  5. 5.

    Smith SE, Facelli E, Pope S, Smith FA (2010) Plant performance in stressful environments: interpreting new and established knowledge of the roles of arbuscular mycorrhizas. Plant Soil 326(1–2):3–20

    CAS  Google Scholar 

  6. 6.

    Lau JA, Lennon JT (2012) Rapid responses of soil microorganisms improve plant fitness in novel environments. Proc Natl Acad Sci 109(35):14058–14062. https://doi.org/10.1073/pnas.1202319109

    Article  PubMed  Google Scholar 

  7. 7.

    Kivlin SN, Emery SM, Rudgers JA (2013) Fungal symbionts alter plant responses to global change. Am J Bot 100(7):1445–1457. https://doi.org/10.3732/ajb.1200558

    Article  PubMed  Google Scholar 

  8. 8.

    O’Brien MJ, Pugnaire FI, Rodríguez-Echeverría S, Morillo JA, Martín-Usero F, López-Escoriza A, Aránega DJ, Armas C (2018) Mimicking a rainfall gradient to test the role of soil microbiota for mediating plant responses to drier conditions. Oikos

  9. 9.

    Rajkumar M, Sandhya S, Prasad MNV, Freitas H (2012) Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnol Adv 30(6):1562–1574

    PubMed  CAS  Google Scholar 

  10. 10.

    Afkhami ME, Rudgers JA, Stachowicz JJ (2014) Multiple mutualist effects: conflict and synergy in multispecies mutualisms. Ecology 95(4):833–844

    PubMed  Google Scholar 

  11. 11.

    Lankau RA, Zhu K, Ordonez A (2015) Mycorrhizal strategies of tree species correlate with trailing range edge responses to current and past climate change. Ecology 96(7):1451–1458. https://doi.org/10.1890/14-2419.1

    Article  Google Scholar 

  12. 12.

    Hayward J, Horton TR, Pauchard A, Nuñez MA (2015) A single ectomycorrhizal fungal species can enable a Pinus invasion. Ecology 96(5):1438–1444

    PubMed  Google Scholar 

  13. 13.

    Van Nuland ME, Bailey JK, Schweitzer JA (2017) Divergent plant–soil feedbacks could alter future elevation ranges and ecosystem dynamics. Nat Ecol Evol 1(6):0150

    Google Scholar 

  14. 14.

    Harrison TL, Simonsen AK, Stinchcombe JR, Frederickson ME (2018) More partners, more ranges: generalist legumes spread more easily around the globe. Biol Lett 14(11):20180616

    PubMed  PubMed Central  Google Scholar 

  15. 15.

    Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees SCM, Bakker PAHM (2014) Induced systemic resistance by beneficial microbes. Ann Rev Phytopathol 52:347–375

    CAS  Google Scholar 

  16. 16.

    Hubbard CJ, Li B, McMinn R, Brock MT, Maignien L, Ewers BE, Kliebenstein D, Weinig C (2019) The effect of rhizosphere microbes outweighs host plant genetics in reducing insect herbivory. Molec Ecol 28(7):1801–1811

    CAS  Google Scholar 

  17. 17.

    Anacker BL, Klironomos JN, Maherali H, Reinhart KO, Strauss SY (2014) Phylogenetic conservatism in plant-soil feedback and its implications for plant abundance. Ecol Lett 17(12):1613–1621. https://doi.org/10.1111/ele.12378

    Article  PubMed  Google Scholar 

  18. 18.

    Siefert A, Zillig KW, Friesen ML, Strauss SY (2019) Mutualists stabilize the coexistence of congeneric legumes. Am Nat 193(2):200–212

    PubMed  Google Scholar 

  19. 19.

    Wagner MR, Lundberg DS, Coleman-Derr D, Tringe SG, Dangl JL, Mitchell-Olds T (2014) Natural soil microbes alter flowering phenology and the intensity of selection on flowering time in a wild Arabidopsis relative. Ecol Lett 17(6):717–726. https://doi.org/10.1111/ele.12276

    Article  PubMed  PubMed Central  Google Scholar 

  20. 20.

    O’Brien AM, Sawers RJH, Strauss SY, Ross-Ibarra J (2019) Adaptive phenotypic divergence in an annual grass differs across biotic contexts. Evolution 73:2230–2246. https://doi.org/10.1111/evo.13818

    Article  PubMed  Google Scholar 

  21. 21.

    Heath KD, Burke PV, Stinchcombe JR (2012) Coevolutionary genetic variation in the legume-rhizobium transcriptome. Molec Ecol 21(19):4735–4747. https://doi.org/10.1111/j.1365-294X.2012.05629.x.. ISSN 1365-294X

    Article  Google Scholar 

  22. 22.

    Heath KD, Stinchcombe JR (2014) Explaining mutualism variation: a new evolutionary paradox? Evolution 68(2):309–317

    PubMed  Google Scholar 

  23. 23.

    Rúa MA, Antoninka A, Antunes PM, Chaudhary VB, Gehring C, Lamit LJ et al (2016) Home-field advantage? Evidence of local adaptation among plants, soil, and arbuscular mycorrhizal fungi through meta-analysis. BMC Evol Biol 16:1. https://doi.org/10.1186/s12862-016-0698-9

    Article  Google Scholar 

  24. 24.

    Johnson NC, Wilson GWT, Bowker MA, Wilson JA, Miller RM (2010) Resource limitation is a driver of local adaptation in mycorrhizal symbioses. Proc Natl Acad Sci 107(5):2093–2098. https://doi.org/10.1073/pnas.0906710107

    Article  PubMed  Google Scholar 

  25. 25.

    Thompson JN (2005) The geographic mosaic of coevolution. University of Chicago Press, Chicago

    Google Scholar 

  26. 26.

    Landolt E (1975) Morphological differentiation and geographical distribution of the Lemna Gibba-Lemna Minor Group. Aquat Bot 1:345–363

    Google Scholar 

  27. 27.

    RDSC (2016) Rutgers duckweed stock center Online; https://ruduckweed.org; Accessed 25 Oct 2016

  28. 28.

    Ho KHE (2017) The effects of asexuality and selfing on genetic diversity the efficacy of selection and species persistence. University of Toronto St. George, PhD thesis

    Google Scholar 

  29. 29.

    Liu C, Dai Z, Sun H (2017) Potential of duckweed (Lemna Minor) for removal of nitrogen and phosphorus from water under salt stress. J Environ Manag 187:497–503

    CAS  Google Scholar 

  30. 30.

    Shantz AA, Lemoine NP, Burkepile DE (2016) Nutrient loading alters the performance of key nutrient exchange mutualisms. Ecol Lett 19(1):20–28

    PubMed  Google Scholar 

  31. 31.

    Bulgarelli D, Rott M, Schlaeppi K, van Themaat EVL, Ahmadinejad N, Assenza F, Rauf P, Huettel B, Reinhardt R, Schmelzer E, Peplies J, Gloeckner FO, Amann R, Eickhorst T, Schulze-Lefert P (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488(7409):91–95. https://doi.org/10.1038/nature11336

    Article  PubMed  CAS  Google Scholar 

  32. 32.

    Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, del Rio TG, Edgar RC, Eickhorst T, Ley RE, Hugenholtz P, Tringe SG, Dangl JL (2012) Defining the core Arabidopsis Thaliana root microbiome. Nature 488(7409):86–90. https://doi.org/10.1038/nature11237

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. 33.

    Ishizawa H, Kuroda M, Morikawa M, Ike M (2017) Evaluation of environmental bacterial communities as a factor affecting the growth of duckweed Lemna Minor. Biotechnol Biofuels 10(1):62

    PubMed  PubMed Central  Google Scholar 

  34. 34.

    Yuan Z, Druzhinina IS, Labbé J, Redman R, Qin Y, Rodriguez R, Zhang C, Tuskan GA, Lin F (2016) Specialized microbiome of a halophyte and its role in helping non-host plants to withstand salinity. Sci Rep 6:32467

    PubMed  PubMed Central  CAS  Google Scholar 

  35. 35.

    Nriagu JO, Pacyna JM (1988) Quantitative assessment of worldwide contamination of air, water and soils by trace metals. Nature 333(6169):134

    PubMed  CAS  Google Scholar 

  36. 36.

    Dugan HA, Bartlett SL, Burke SM, Doubek JP, Krivak-Tetley FE, Skaff NK, Summers JC, Farrell KJ, McCullough IM, Morales-Williams AM et al (2017) Salting our freshwater lakes. Proc Natl Acad Sci 114(17):4453–4458

    PubMed  CAS  Google Scholar 

  37. 37.

    Rochman CM (2018) Microplastics research—from sink to source. Science 360(6384):28–29

    PubMed  CAS  Google Scholar 

  38. 38.

    Avis TJ, Gravel V, Antoun H, Tweddell RJ (2008) Multifaceted beneficial effects of rhizosphere microorganisms on plant health and productivity. Soil Biol Biochem 40(7):1733–1740

    CAS  Google Scholar 

  39. 39.

    Dijkstra FA, Carrillo Y, Pendall E, Morgan JA (2013) Rhizosphere priming: a nutrient perspective. Front Microbiol 4:216

    PubMed  PubMed Central  CAS  Google Scholar 

  40. 40.

    Janzen DH (1985) The natural history of mutualisms. The biology of mutualism: ecology and evolution, pp 40–99

  41. 41.

    Batstone RT, Dutton EM, Wang D, Yang M, Frederickson ME (2016) The evolution of symbiont preference traits in the model legume Medicago Truncatula. New Phytologist, in press

  42. 42.

    Madhaiyan M, Poonguzhali S, Sa T (2007) Metal tolerating methylotrophic bacteria reduces nickel and cadmium toxicity and promotes plant growth of tomato (Lycopersicon Esculentum L.) Chemosphere 69(2):220–228

    PubMed  CAS  Google Scholar 

  43. 43.

    Braud A, Jézéquel K, Bazot S, Lebeau T (2009) Enhanced phytoextraction of an agricultural Cr-and Pb-contaminated soil by bioaugmentation with siderophore-producing bacteria. Chemosphere 74(2):280–286

    PubMed  Google Scholar 

  44. 44.

    Glick BR (2003) Phytoremediation: synergistic use of plants and bacteria to clean up the environment. Biotechnol Adv 21(5):383–393

    PubMed  CAS  Google Scholar 

  45. 45.

    Mueller UG, Sachs JL (2015) Engineering microbiomes to improve plant and animal health. Trends Microbiol 23(10):606–617

    PubMed  CAS  Google Scholar 

  46. 46.

    Mo SC, Choi DS, Robinson JW (1989) Uptake of mercury from aqueous solution by duckweed: the effects of pH, copper and humic acid. J Environ Sci Health Part A 24(2):135–146

    Google Scholar 

  47. 47.

    Stout L, Nüsslein K (2010) Biotechnological potential of aquatic plant–microbe interactions. Curr Opin Biotechnol 21(3):339–345

    PubMed  CAS  Google Scholar 

  48. 48.

    Gatidou G, Oursouzidou M, Stefanatou A, Stasinakis AS (2017) Removal mechanisms of benzotriazoles in duckweed Lemna Minor wastewater treatment systems. Sci Total Environ 596:12–17

    PubMed  Google Scholar 

  49. 49.

    Dirilgen N, Inel Y (1994) Effects of zinc and copper on growth and metal accumulation in duckweed, Lemna Minor. Bull Environ Contamin Toxicol 53(3):442–449

    CAS  Google Scholar 

  50. 50.

    Radić S, Babić M, Škobić D, Roje V, Pevalek-Kozlina B (2010) Ecotoxicological effects of aluminum and zinc on growth and antioxidants in Lemna Minor l. Ecotoxicol Environ Safety 73(3):336–342

    PubMed  Google Scholar 

  51. 51.

    Jayasri MA, Suthindhiran K (2017) Effect of zinc and lead on the physiological and biochemical properties of aquatic plant Lemna Minor: its potential role in phytoremediation. Appl Water Sci 7(3):1247–1253

    CAS  Google Scholar 

  52. 52.

    Göbel P, Dierkes C, Coldewey WG (2007) Storm water runoff concentration matrix for urban areas. J Contamin Hydrol 91(1):26–42

    Google Scholar 

  53. 53.

    Glooschenko V, Weller WF, Smith PGR, Alvo R, Archbold JHG (1992) Amphibian distribution with respect to pond water chemistry near Sudbury, Ontario. Can J Fish Aquat Sci 49(S1):114–121

    CAS  Google Scholar 

  54. 54.

    Miller PA, Munkittrick KR, Dixon DG (1992) Relationship between concentrations of copper and zinc in water, sediment, benthic invertebrates, tissues of white sucker (Catostomus Commersoni) at metal-contaminated sites. Can J Fish Aquat Sci 49(5):978–984

    CAS  Google Scholar 

  55. 55.

    Heijerick DG, De Schamphelaere KAC, Janssen CR (2002) Predicting acute zinc toxicity for Daphnia Magna as a function of key water chemistry characteristics: development and validation of a biotic ligand model. Environ Toxicol Chem 21(6):1309–1315

    PubMed  CAS  Google Scholar 

  56. 56.

    Zhao Y, Fang Y, Jin Y, Huang J, Ma X, He K, He Z, Wang F, Zhao H (2015) Microbial community and removal of nitrogen via the addition of a carrier in a pilot-scale duckweed-based wastewater treatment system. Bioresour Technol 179:549–558

    PubMed  CAS  Google Scholar 

  57. 57.

    O’Brien AM, Yu ZH, D-y Luo J, Laurich E P, Frederickson M (2019) Resilience to multiple stressors in an aquatic plant and its microbiome. bioRxiv, https://doi.org/10.1101/726653, https://www.biorxiv.org/content/early/2019/08/06/726653

  58. 58.

    Van Steveninck RFM, Van Steveninck ME, Wells AJ, Fernando DR (1990) Zinc tolerance and the binding of zinc as zinc phytate in Lemna Minor. X-ray microanalytical evidence. J Plant Physiol 137(2):140–146

    Google Scholar 

  59. 59.

    Balen B, Tkalec M, Šikić S, Tolić S, Cvjetko P, Pavlica M, Vidaković-Cifrek ž (2011) Biochemical responses of Lemna Minor experimentally exposed to cadmium and zinc. Ecotoxicology 20(4):815–826

    PubMed  CAS  Google Scholar 

  60. 60.

    Zhao Y, Fang Y, Jin Y, Huang J, Bao S, Fu T, He Z, Wang F, Wang M, Zhao H (2014) Pilot-scale comparison of four duckweed strains from different genera for potential application in nutrient recovery from wastewater and valuable biomass production. Plant Biol 17:82–90. https://doi.org/10.1111/plb.12204

    Article  PubMed  CAS  Google Scholar 

  61. 61.

    Sowjanya Sree K, Adelmann K, Garcia C, Lam E, Appenroth K-J (2015) Natural variance in salt tolerance and induction of starch accumulation in duckweeds. Planta 241(6):1395–1404

    PubMed  Google Scholar 

  62. 62.

    Ziegler P, Adelmann K, Zimmer S, Schmidt C, Appenroth K-J (2015) Relative in vitro growth rates of duckweeds (Lemnaceae) – the most rapidly growing higher plants. Plant Biol 17:33–41. https://doi.org/10.1111/plb.12184. ISSN 1438-8677

    Article  PubMed  Google Scholar 

  63. 63.

    Krazčič B, Slekovec-Golob M, Nemec J (1995) Promotion of flowering by Mn-EDDHA in the photoperiodically neutral plant Spirodela Polyrrhiza (l.) Schleiden. J Plant Physiol 147(3):397–400

    Google Scholar 

  64. 64.

    Rejmankova E, Blackwell M, Culley DD (1986) Dynamics of fungal infection in duckweeds (Lemnaceae). Veröffentlichungen des Geobotanischen Institutes der ETH, Stiftung Rübel Zürich 87:178–189

    Google Scholar 

  65. 65.

    Goldsborough LG (1993) Diatom ecology in the phyllosphere of the common duckweed (Lemna Minor l.) Hydrobiologia 269(1):463–471

    Google Scholar 

  66. 66.

    Duong TP, Tiedje JM (1985) Nitrogen fixation by naturally occurring duckweed–cyanobacterial associations. Canad J Microbiol 31(4):327–330

    CAS  Google Scholar 

  67. 67.

    Underwood GJC, Baker JH (1991) The effect of various aquatic bacteria on the growth and senescence of duckweed (Lemna Minor). J Appl Bacteriol 70(3):192–196

    Google Scholar 

  68. 68.

    Stout LM, Dodova EN, Tyson JF, Nüsslein K (2010) Phytoprotective influence of bacteria on growth and cadmium accumulation in the aquatic plant Lemna Minor. Water Res 44(17):4970–4979

    PubMed  CAS  Google Scholar 

  69. 69.

    Rappé MS, Giovannoni SJ (2003) The uncultured microbial majority. Ann Rev Microbiol 57(1):369–394

    Google Scholar 

  70. 70.

    Thijs S, De Beeck MO, Beckers B, Truyens S, Stevens V, Van Hamme JD, Weyens N, Vangronsveld J (2017) Comparative evaluation of four bacteria-specific primer pairs for 16s rRNA gene surveys. Front Microbiol 8:494

    PubMed  PubMed Central  Google Scholar 

  71. 71.

    Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet C, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F et al (2018) QIIME 2: reproducible, interactive, scalable and extensible microbiome data science. Technical report, PeerJ Preprints

  72. 72.

    McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P (2012) An improved greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6(3):610

    PubMed  CAS  Google Scholar 

  73. 73.

    R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/. Version 3.1.1

    Google Scholar 

  74. 74.

    Dray S, Dufour A -B (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22(4):1–20. https://doi.org/10.18637/jss.v022.i04

    Article  Google Scholar 

  75. 75.

    Liskco ZJ, Struger J (1996) Trace metals contamination of urban streams and stormwater detention ponds. In: James W (ed) Advances in modeling the management of stormwater impacts, chapter 17. CRC Press, pp 269–278

  76. 76.

    Ontario Ministry of the Environment (2011) Technical memorandum: an analysis of nutrients and select metals within wastewater (pond discharges). Technical report, Southwestern Regional Office, 03

  77. 77.

    Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to ImageJ: 25 years of image analysis. Nat Methods 9(7):671–675

    PubMed  PubMed Central  CAS  Google Scholar 

  78. 78.

    Newton RJ (1977) Abscisic acid effects on fronds and roots of Lemna Minor l. Am J Bot 64(1):45–49

    CAS  Google Scholar 

  79. 79.

    Chu C, Mandrak NE, Minns CK (2005) Potential impacts of climate change on the distributions of several common and rare freshwater fishes in Canada. Divers Distrib 11(4):299–310

    Google Scholar 

  80. 80.

    Herb WR, Mohseni O, Stefan HG (2009) Simulation of temperature mitigation by a stormwater detention pond 1. JAWRA J Am Water Resour Assoc 45(5):1164–1178

    Google Scholar 

  81. 81.

    Comte L, Buisson L, Daufresne M, Grenouillet G (2013) Climate-induced changes in the distribution of freshwater fish: observed and predicted trends. Freshw Biol 58(4):625–639

    Google Scholar 

  82. 82.

    Adamsen FG, Pinter PJ, Barnes EM, LaMorte RL, Wall GW, Leavitt SW, Kimball BA (1999) Measuring wheat senescence with a digital camera. Crop Sci 39(3):719–724

    Google Scholar 

  83. 83.

    Keenan TF, Darby B, Felts E, Sonnentag O, Friedl MA, Hufkens K, O’Keefe J, Klosterman S, William Munger J, Toomey M et al (2014) Tracking forest phenology and seasonal physiology using digital repeat photography: a critical assessment. Ecol Appl 24(6):1478–1489

    PubMed  CAS  Google Scholar 

  84. 84.

    Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw 33(2):1–22. Version 2.22.1

    Google Scholar 

  85. 85.

    Spiegelhalter DJ, Best NG, Carlin BP, Van Der Linde A (2002) Bayesian measures of model complexity and fit. J R Stat Soc: Series B (Stat Methodol) 64(4):583–639. https://doi.org/10.1111/1467-9868.00353

    Article  Google Scholar 

  86. 86.

    Volkmer B, Heinemann M (2011) Condition-dependent cell volume and concentration of Escherichia Coli to facilitate data conversion for systems biology modeling. PloS one 6(7):e23126

    PubMed  PubMed Central  CAS  Google Scholar 

  87. 87.

    Friesen ML, Porter SS, Stark SC, von Wettberg EJ, Sachs JL, Martinez-Romero E (2011) Microbially mediated plant functional traits. Ann Rev Ecol Evol System 42:23–46

    Google Scholar 

  88. 88.

    Radić S, Stipaničev D, Cvjetko P, Mikelić IL, Rajčić MM, Širac S, Pevalek-Kozlina B, Pavlica M (2009) Ecotoxicological assessment of industrial effluent using duckweed (Lemna Minor l.) as a test organism. Ecotoxicology 19:1. https://doi.org/10.1007/s10646-009-0408-0. ISSN 1573–3017

    Article  CAS  Google Scholar 

  89. 89.

    Mohan BS, Hosetti BB (1999) Aquatic plants for toxicity assessment. Environ Res 81(4):259–274

    PubMed  CAS  Google Scholar 

  90. 90.

    Naumann B, Eberius M, Appenroth K-J (2007) Growth rate based dose–response relationships and EC-values of ten heavy metals using the duckweed growth inhibition test (ISO 20079) with Lemna Minor l. clone st. J Plant Physiol 164(12):1656–1664

    PubMed  CAS  Google Scholar 

  91. 91.

    Henke R, Eberius M, Appenroth K-J (2011) Induction of frond abscission by metals and other toxic compounds in Lemna Minor. Aquatic Toxicol 101(1):261–265

    CAS  Google Scholar 

  92. 92.

    Prati D, Schmid B (2000) Genetic differentiation of life-history traits within populations of the clonal plant Ranunculus Reptans. Oikos 90(3):442–456

    Google Scholar 

  93. 93.

    Agrawal AA, Conner JK, Rasmann S (2010) Tradeoffs and negative correlations in evolutionary ecology. Evolution since Darwin: the first 150:243–268

    Google Scholar 

  94. 94.

    Albert CH, Thuiller W, Yoccoz NG, Douzet R, Aubert S, Lavorel S (2010) A multi-trait approach reveals the structure and the relative importance of intra-vs. interspecific variability in plant traits. Funct Ecol 24 (6):1192–1201

    Google Scholar 

  95. 95.

    Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68(1):1–13. https://doi.org/10.1111/j.1574-6941.2009.00654.x

    Article  PubMed  CAS  Google Scholar 

  96. 96.

    Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417(6884):67–70. https://doi.org/10.1038/417067a

    Article  PubMed  CAS  Google Scholar 

  97. 97.

    Bailey JK, Schweitzer JA (2016) Functional ecology special feature: ecosystems, evolution, and plant-soil feedbacks. Funct Ecol 30:1025–1266

    Google Scholar 

  98. 98.

    Preston GM (2004) Plant perceptions of plant growth-promoting Pseudomonas. Philos Trans R Soc London Series B: Biol Sci 359(1446):907–918

    CAS  Google Scholar 

  99. 99.

    Friesen ML (2012) Widespread fitness alignment in the legume–rhizobium symbiosis. N Phytol 194(4):1096–1111

    Google Scholar 

  100. 100.

    Weese DJ, Heath KD, Dentinger B, Lau JA (2015) Long-term nitrogen addition causes the evolution of less-cooperative mutualists. Evolution 69(3):631–642

    PubMed  CAS  Google Scholar 

  101. 101.

    Desianti N (2012) Interactions between duckweeds and their diatom epiphytes. University of Oklahoma, PhD thesis

    Google Scholar 

  102. 102.

    Zuberer DA (1982) Nitrogen fixation (acetylene reduction) associated with duckweed (Lemnaceae) mats. Appl Environ Microbiol 43(4):823–828

    PubMed  PubMed Central  CAS  Google Scholar 

  103. 103.

    Eckardt NA, Biesboer DD (1988) Ecological aspects of nitrogen fixation (acetylene reduction) associated with plants of a Minnesota wetland community. Canad J Botany 66(7):1359–1363

    Google Scholar 

  104. 104.

    Ishizawa H, Kuroda M, Ike M (2017) Draft genome sequence of Aquitalea Magnusonii strain H3, a plant growth-promoting bacterium of duckweed (Lemna Minor). Genome Announ 5(33):e00812–17

    Google Scholar 

  105. 105.

    Sachs JL, Mueller UG, Wilcox TP, Bull JJ (2004) The evolution of cooperation. Q Rev Biol 79 (2):135–160. https://doi.org/10.1086/383541

    Article  PubMed  Google Scholar 

  106. 106.

    Mkandawire M, Dudel EG (2007) Are Lemna SPP. effective phytoremediation agents. Bioremed, Biodiver Bioavailab 1(1):56– 71

    Google Scholar 

  107. 107.

    Ziegler P, Sree KS, Appenroth K-J (2016) Duckweeds for water remediation and toxicity testing. Toxicol Environ Chem 98(10):1127–1154

    CAS  Google Scholar 

  108. 108.

    Sekomo CB, Rousseau DPL, Saleh SA, Lens PNL (2012) Heavy metal removal in duckweed and algae ponds as a polishing step for textile wastewater treatment. Ecol Eng 44:102–110

    Google Scholar 

  109. 109.

    Uysal Y (2013) Removal of chromium ions from wastewater by duckweed, Lemna Minor l. by using a pilot system with continuous flow. J Hazard Mater 263:486–492

    PubMed  CAS  Google Scholar 

  110. 110.

    Sasmaz M, Topal EIA, Obek E, Sasmaz A (2015) The potential of Lemna Gibba l. and Lemna Minor l. to remove Cu, Pb, Zn, and as in gallery water in a mining area in Keban, Turkey. J Environ Manag 163:246–253

    CAS  Google Scholar 

  111. 111.

    Baciak M, Sikorski Ł, Piotrowicz-Cieślak AI, Adomas B (2016) Content of biogenic amines in Lemna Minor (common duckweed) growing in medium contaminated with tetracycline. Aquat Toxicol 180:95–102

    PubMed  CAS  Google Scholar 

  112. 112.

    Gomes MP, Gonćalves C A, de Brito JCM, Souza AM, da Silva Cruz FV, Bicalho EM, Figueredo CC, Garcia QS (2017) Ciprofloxacin induces oxidative stress in duckweed (Lemna Minor l.): implications for energy metabolism and antibiotic-uptake ability. J Hazard Mater 328:140–149

    PubMed  CAS  Google Scholar 

  113. 113.

    Toyama T, Sei K, Yu N, Kumada H, Inoue D, Hoang H, Soda S, Chang Y-C, Kikuchi S, Fujita M et al (2009) Enrichment of bacteria possessing catechol dioxygenase genes in the rhizosphere of Spirodela Polyrrhiza: a mechanism of accelerated biodegradation of phenol. Water Res 43(15):3765–3776

    PubMed  CAS  Google Scholar 

  114. 114.

    Luminita Sobariu D, Fertu DIT, Diaconu M, Pavel LV, Hlihor R -M, Drǎgoi E N, Curteanu S, Lenz M, François-Xavier Corvini P, Gavrilescu M (2017) Rhizobacteria and plant symbiosis in heavy metal uptake and its implications for soil bioremediation. Biotechnol 39:125–134

    Google Scholar 

  115. 115.

    Burd GI, George Dixon D, Glick BR (2000) Plant growth-promoting bacteria that decrease heavy metal toxicity in plants. Canad J Microbiol 46(3):237–245

    CAS  Google Scholar 

  116. 116.

    Visioli G, D’Egidio S, Sanangelantoni AM (2015) The bacterial rhizobiome of hyperaccumulators: future perspectives based on omics analysis and advanced microscopy. Front Plant Sci 5:752

    PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The authors would like to thank D. Sinton and B. Nguyen for engineering solutions improving our experimental setup and members of the Frederickson lab for discussion.

Funding

This work was funded by the Natural Sciences and Engineering Council of Canada (NSERC), through a Discovery Grant to MEF (RGPIN-2015-06742) and a Canada Graduate Scholarship to JL. EL was supported by the University of Toronto Centre for Global Change Science.

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JL, EL, MEF, and AMO executed collections. AMO and JL ran the experiment and collected data. AMO performed analyses and provided the first draft. All contributed to study design, revised the manuscript, and gave approval for publication.

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Correspondence to Anna M. O’Brien.

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The authors declare that they have no conflict of interest.

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O’Brien, A.M., Laurich, J., Lash, E. et al. Mutualistic Outcomes Across Plant Populations, Microbes, and Environments in the Duckweed Lemna minor. Microb Ecol 80, 384–397 (2020). https://doi.org/10.1007/s00248-019-01452-1

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Keywords

  • Biotic interactions
  • Freshwater ecosystems
  • Duckweed
  • Host–microbe interactions
  • Phytoremediation
  • Zinc