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Depicting Temporal, Functional, and Phylogenetic Patterns in Estuarine Diazotrophic Communities from Environmental DNA and RNA

  • Microbiology of Aquatic Systems
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Abstract

Seasonally nitrogen-limited and phosphorus-replete temperate coastal waters generally host dense and diverse diazotrophic communities. Despite numerous studies in marine systems, little is known about diazotrophs and their functioning in oligohaline estuarine environments. Here we applied a combination of nifH transcript and metagenomic shotgun sequencing approaches to investigate temporal shifts in taxonomic composition and nifH activity of size-fractionated diazotrophic communities in a shallow and mostly freshwater coastal lagoon. Patterns in active nifH phylotypes exhibited a clear seasonal succession, which reflected their different tolerances to temperature change and nitrogen (N) availability. Thus, in spring, heterotrophic diazotrophs (Proteobacteria) dominated the nifH phylotypes, while increasing water temperature and depletion of inorganic N fostered heterocystous Cyanobacteria in summer. Metagenomic data demonstrated four main N-cycling pathways and three of them with a clear seasonal pattern: denitrification (spring) → N2 fixation (summer) → assimilative NO3− reduction (fall), with NH4+ uptake into cells occurring across all seasons. Although a substantial denitrification signal was observed in spring, it could have originated from the re-suspended benthic rather than planktonic community. Our results contribute to a better understanding of the realized genetic potential of pelagic N2 fixation and its seasonal dynamics in oligohaline estuarine ecosystems, which are natural coastal biogeochemical reactors.

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References

  1. Carstensen J, Sánchez-Camacho M, Duarte CM, Krause-Jensen D, Marbà N (2011) Connecting the dots: responses of coastal ecosystems to changing nutrient concentrations. Environ Sci Technol 45(21):9122–9132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Gazeau F, Smith SV, Gentili B, Frankignoulle M, Gattuso JP (2004) The European coastal zone: characterization and first assessment of ecosystem metabolism. Estuar Coast Shelf Sci 60(4):673–694

    Article  CAS  Google Scholar 

  3. Boyer EW, Howarth RW (2008) Nitrogen fluxes from rivers to the coastal oceans. In: Capone DG, Bronk DA, Mulholland MR, Carpenter EJ (eds) Nitrogen in the marine environment2nd edn. Academic Press, San Diego, pp 1565–1587

    Chapter  Google Scholar 

  4. Bukaveckas PA, Beck M, Devore D, Lee WM (2018) Climatic variability and its role in regulating C, N and P retention in the James River Estuary. Estuar Coast Shelf Sci 205:161–173

    Article  CAS  Google Scholar 

  5. Vybernaite-Lubiene I, Zilius M, Giordani G, Petkuviene J, Vaiciute D, Bukaveckas PA, Bartoli M (2017) Effect of algal blooms on retention of N, Si and P in Europe’s largest coastal lagoon. Estuar Coast Shelf Sci 194:217–228. https://doi.org/10.1016/j.ecss.2017.06.020

    Article  CAS  Google Scholar 

  6. Howarth RW, Marino R (2006) Nitrogen as the limiting nutrient for eutrophication in coastal marine ecosystems: evolving views over three decades. Limnol Oceanogr 51(1):364–376

    Article  CAS  Google Scholar 

  7. Huisman JM, Matthijs HCP, Visser PM (2005) Harmful cyanobacteria. Springer aquatic ecology series3rd edn. Springer, Dordrecht, p 243

    Google Scholar 

  8. Bentzon-Tilia M, Traving SJ, Mantikci M, Knudsen-Leerbeck H, Hansen JLS, Markager S, Riemann L (2015) Significant N2 fixation by heterotrophs, photoheterotrophs and heterocystous cyanobacteria in two temperate estuaries. ISME J 9:273–285. https://doi.org/10.1038/ismej.2014.119

    Article  CAS  PubMed  Google Scholar 

  9. Boström KH, Riemann L, Zweifel UL, Hagström Å (2007) Nodularia sp. nifH gene transcripts in the Baltic Sea proper. J Plankton Res 29(4):391–399. https://doi.org/10.1093/plankt/fbm01

    Article  Google Scholar 

  10. Farnelid H, Bentzon-Tilia M, Andersson AF, Bertilsson S, Jost G, Labrenz M, Jürgens K, Riemann L (2013) Active nitrogen-fixing heterotrophic bacteria at and below the chemocline of the central Baltic Sea. ISME J 7:1413–1423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Klawonn I, Nahar N, Walve J, Andersson OM, Svedén JB, Littmann S, Whitehouse MJ, Kuypers MMM, Ploug H (2016) Cell-specific nitrogen- and carbon-fixation of cyanobacteria in a temperate marine system (Baltic Sea). Environ Microbiol 18(12):4596–4609. https://doi.org/10.1111/1462-2920.13557

    Article  CAS  PubMed  Google Scholar 

  12. Marino R, Chan F, Howarth R, Pace M, Likens GE (2002) Ecological and biogeochemical interactions constrain planktonic nitrogen fixation in estuaries. Ecosystems 5(7):719–725. https://doi.org/10.1007/s10021-002-0176-7

    Article  CAS  Google Scholar 

  13. Staal M, Meysman FJ, Stal LJ (2003) Temperature excludes N2-fixing heterocystous cyanobacteria in the tropical oceans. Nature 425(6957):504–507

    Article  CAS  PubMed  Google Scholar 

  14. Riemann L, Farnelid H, Steward GF (2010) Nitrogenase genes in non-cyanobacterial plankton: prevalence, diversity and regulation in marine waters. Aquat Microb Ecol 61:235–247. https://doi.org/10.3354/ame01431

    Article  Google Scholar 

  15. Farnelid H, Turk-Kubo K, Muñoz-Marín MC, Zehr JP (2016) New insights into the ecology of the globally significant uncultured nitrogen-fixing symbiont UCYN-A. Aquat Microb Ecol 77:125–138. https://doi.org/10.3354/ame01794

    Article  Google Scholar 

  16. Zani S, Mellon MT, Collier JL, Zehr JP (2000) Expression of nifH genes in natural microbial assemblages in Lake George, New York, detected by reverse transcriptase PCR. Appl Environ Microbiol 66(7):3119–3124. https://doi.org/10.1128/AEM.66.7.3119-3124.2000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Zehr JP, Jenkins BD, Short SM, Steward GF (2003) Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ Microbiol 7:539–554

    Article  Google Scholar 

  18. Bentzon-Tilia M, Sverin I, Hansen LH, Hansen H, Riemann L (2015) Genomic and ecophysiology of heterotrophic N-fixing bacteria isolated from estuarine surface water. mBio 6(4):1–11. e00929-15. https://doi.org/10.1128/mBio.00929-15

    Article  CAS  Google Scholar 

  19. Paerl HW (1990) Physiological ecology and regulation of N2 fixation in natural waters. In: Marshall KC (ed) Advances in microbial ecology, 11. Springer, Boston, pp 305–344

    Chapter  Google Scholar 

  20. Zilius M, Bartoli M, Bresciani M, Katarzyte M, Ruginis T, Petkuviene J, Lubiene I, Giardino C, Bukaveckas PA, de Wit R, Razinkovas-Baziukas A (2014) Feedback mechanisms between cyanobacterial blooms, transient hypoxia, and benthic phosphorus regeneration in shallow coastal environments. Estuar Coasts 37(3):680–694

    Article  CAS  Google Scholar 

  21. Zilius M, Vybernaite-Lubiene I, Vaiciute D, Petkuviene J, Zemlys P, Liskow I, Voss M, Bartoli M, Bukaveckas PA (2018) The influence of cyanobacteria blooms on the attenuation of nitrogen throughputs in a Baltic coastal lagoon. Biogeochemistry 141(2):143–165. https://doi.org/10.1007/s10533-018-0508-0

    Article  CAS  Google Scholar 

  22. Lu J, Zhu B, Struewing I, Xu N, Duan S (2019) Nitrogen–phosphorus-associated metabolic activities during the development of a cyanobacterial bloom revealed by metatranscriptomics. Sci Rep 9:2480. https://doi.org/10.1038/s41598-019-38481-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Adam B, Klawonn I, Svedén J et al (2016) N2-fixation, ammonium release and N-transfer to the microbial and classical food web within a plankton community. ISME J 10:450–459. https://doi.org/10.1038/ismej.2015.126

    Article  CAS  PubMed  Google Scholar 

  24. Zemlys P, Ferrarin C, Umgiesser G, Gulbinskas S, Bellafiore D (2013) Investigation of saline water intrusions into the Curonian Lagoon (Lithuania) and two-layer flow in the Klaipėda Strait using finite element hydrodynamic model. Ocean Sci 9(3):573–584. https://doi.org/10.5194/os-9-573-2013

    Article  Google Scholar 

  25. Olenina I (2012) Identification of algae species in the Curonian Lagoon. SUBMARINE Rep 17A:1–14

    Google Scholar 

  26. Samuiloviene A, Bartoli M, Bonaglia S, Cardini U, Vybernaite-Lubiene I, Marzocchi U, Petkuviene J, Politi T, Zaiko A, Zilius M (2019) The effect of chironomid larvae on nitrogen cycling and microbial communities in soft sediments. Water 11:1931. https://doi.org/10.3390/w1109193

    Article  CAS  Google Scholar 

  27. Milani C, Hevia A, Foroni E, Duranti S, Turroni F, Lugli GA, Sanchez B, Martín R, Gueimonde M, van Sinderen D, Margolles A, Ventura M (2013) Assessing the fecal microbiota: an optimized ion torrent 16S rRNA gene-based analysis protocol. PLoS One 8(7):e68739. https://doi.org/10.1371/journal.pone.0068739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Zehr JP, Turner PJ (2001) Nitrogen fixation: Nitrogenase genes and gene expression. Methods Microbiol 30:271–286. https://doi.org/10.1016/S0580-9517(01)30049-1

    Article  CAS  Google Scholar 

  29. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the Miseq Illumina sequencing platform. Appl Environ Microbiol 79:5112–5120. https://doi.org/10.1128/AEM.01043-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359. https://doi.org/10.1038/nmeth.1923

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17:10–12. https://doi.org/10.14806/ej.17.1.200

  32. Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods 13(7):581–583. https://doi.org/10.1038/nmeth.3869

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Gaby JC, Buckley DH (2014) A comprehensive aligned nifH gene database: a multipurpose tool for studies of nitrogen-fixing bacteria. Database 2014:bau001. https://doi.org/10.1093/database/bau001

  34. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Andrews S (2010) FastQC: a quality control tool for high throughput sequence data. Available online at http://www.bioinformatics.babraham.ac.uk/projects/fastqc

  36. Ewels P, Magnusson M, Käller M, Lundin S (2016) MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinformatics 32:3047–3048. https://doi.org/10.1093/bioinformatics/btw354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Li D, Luo R, Liu CM, Leung CM, Ting HF, Sadakane K, Yamashita H, Lam TW (2016) MEGAHIT v1.0: a fast and scalable metagenome assembler driven by advanced methodologies and community practices. Methods 102:3–11. https://doi.org/10.1016/j.ymeth.2016.02.020

    Article  CAS  PubMed  Google Scholar 

  38. Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068–2069. https://doi.org/10.1093/bioinformatics/btu153

    Article  CAS  PubMed  Google Scholar 

  39. Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, Hauser LJ (2010) Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11:119. https://doi.org/10.1186/1471-2105-11-119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol Res 215:403–410

    Article  CAS  Google Scholar 

  41. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079. https://doi.org/10.1093/bioinformatics/btp35

    Article  PubMed  PubMed Central  Google Scholar 

  42. Anders S, Pyl PT, Huber W (2015) HTSeq--a Python framework to work with high-throughput sequencing data. Bioinformatics 31:166–169. https://doi.org/10.1093/bioinformatics/btu638

    Article  CAS  PubMed  Google Scholar 

  43. Smid M, Coebergh van den Braak RRJ, van de Werken HJG, van Riet J, van Galen A, de Weerd V et al (2018) Gene length corrected trimmed mean of M-values (GeTMM) processing of RNA-seq data performs similarly in intersample analyses while improving intrasample comparisons. Bioinformatics 19:236. https://doi.org/10.1186/s12859-018-2246-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Grasshoff K, Kremling K, Erhardt M (1999) Methods of seawater analysis. Wiley-VCH, Weinheim

    Book  Google Scholar 

  45. Koroleff F (1983) Determination of phosphorus. In: Grasshoff K, Ehrhardt M, Kremling K (eds) Methods of seawater analysis2nd edn. Weinheim, Verlag Chemie, pp 125–132

    Google Scholar 

  46. Cauwet G (1999) Determination of dissolved organic carbon and nitrogen by high temperature combustion. In: Grasshoff K, Kremling K, Ehrhardt M (eds) Methods of seawater analysis. Wiley-VCH Verlag GmbH, Weinheim, pp 407–420

    Chapter  Google Scholar 

  47. McMurdie PJ, Holmes S (2013) Phyloseq: an R package for reproducibleinteractive analysis and graphics of microbiome census data. PLoS One 8:e61217. https://doi.org/10.1371/journal.pone.0061217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Oksanen J, Blanchet FG, Friendly M et al (2019) Vegan: community ecology package. Retrieved from https://cran.r-project.org/package=vegan

  49. Olofsson M, Suikkanen S, Kobos J, Wasmund N, Karlson B (2020) Basin-specific changes in filamentous cyanobacteria community composition across four decades in the Baltic Sea. Harmful Algae 91:101685. https://doi.org/10.1016/j.hal.2019.101685

    Article  CAS  PubMed  Google Scholar 

  50. Shao Y, Chung BS, Lee SS, Park W, Lee S-S, Jeon CO (2009) Zoogloea caeni sp. nov., a floc-forming bacterium isolated from activated sludge. Int J Syst Evol Microbiol 59(3):526–530. https://doi.org/10.1099/ijs.0.65670-0

    Article  CAS  PubMed  Google Scholar 

  51. Srinivas TN, Kumar A, Sasikala C, Ramana CV, Süling J, Imhoff JF (2006) Rhodovulum marinum sp. nov., a novel phototrophic purple non-sulfur alphaproteobacterium from marine tides of Visakhapatnam, India. Int J Syst Evol Microbiol 56:1651–1656

    Article  CAS  PubMed  Google Scholar 

  52. Man-Aharonovich D, Kress N, Zeev EB, Berman-Frank I, Béjà O (2007) Molecular ecology of nifH genes and transcripts in the eastern Mediterranean Sea. Environ Microbiol 9(9):2354–2363. https://doi.org/10.1111/j.1462-2920.2007.01353.x

    Article  CAS  PubMed  Google Scholar 

  53. Carstensen J, Conley DJ, Almroth-Rosell E, Asmala E, Bonsdorff E, Fleming-Lehtinen V, Gustafsson BG, Gustafsson C, Heiskanen AS, Janas U, Norkko A, Slomp C, Villnäs A, Voss M, Zilius M (2020) Factors regulating the coastal nutrient filter in the Baltic Sea. Ambio 49:1194–1210. https://doi.org/10.1007/s13280-019-01282-y

    Article  CAS  PubMed  Google Scholar 

  54. Bonaglia S, Klawonn I, De Brabandere L, Deutsch B, Thamdrup B, Brüchert V (2016) Denitrification and DNRA at the Baltic Sea oxic–anoxic interface: substrate spectrum and kinetics. Limnol Oceanogr 61(5):1900–1915

    Article  Google Scholar 

  55. Severin I, Bentzon-Tilia M, Moisander PH, Riemann L (2015) Nitrogenase expression in estuarine bacterioplankton influenced by organic carbon and availability of oxygen. FEMS Microbiol Lett 362(14):fnv105. https://doi.org/10.1093/femsle/fnv105

    Article  CAS  PubMed  Google Scholar 

  56. Benavides M, Martias C, Elifantz H, Berman-Frank I, Dupouy C, Bonnet S (2018) Dissolved organic matter influences N2 fixation in the new Caledonian Lagoon (Western Tropical South Pacific). Front Mar Sci 5:89. https://doi.org/10.3389/fmars.2018.00089

    Article  Google Scholar 

  57. Hoikkala L, Tammert H, Lignell R, Eronen-Rasimus E, Spilling K, Kisand V (2016) Autochthonous dissolved organic matter drives bacterial community composition during a bloom of filamentous cyanobacteria. Front Mar Sci 3:111. https://doi.org/10.3389/fmars.2016.00111

    Article  Google Scholar 

  58. Laamanen M, Kuosa H (2005) Annual variability of biomass and heterocysts of the N2 -fixing cyanobacterium Aphanizomenon flos-aquae in the Baltic Sea with reference to Anabaena spp. and Nodularia spumigena. Boreal Environ Res 10(1):19–30

    Google Scholar 

  59. Lehtimäki J, Moisander P, Sivonen K, Kononen K (1997) Growth, nitrogen fixation, and nodularin production by two Baltic Sea cyanobacteria. Appl Environ Microbiol 63(5):1647–1656

    Article  PubMed  PubMed Central  Google Scholar 

  60. De Nobel WT, Huisman J, Snoep JL, Mur LR (1997) Competition for phosphorus between the nitrogen-fixing cyanobacteria Anabaena and Aphanizomenon. FEMS Microbiol Ecol 24(3):259–267. https://doi.org/10.1111/j.1574-6941.1997.tb00443.x

    Article  Google Scholar 

  61. Schoffelen JN, Mohr W, Ferdelman G, Littmann S, Duerschlag J, Zubkov MV, Ploug H, Kuypers MMM (2018) Single-cell imaging of phosphorus uptake shows that key harmful algae rely on different phosphorus sources for growth. Sci Rep 8:17182. https://doi.org/10.1038/s41598-018-35310-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Johnston AWB, Li Y, Ogilvie L (2007) Metagenomic marine nitrogen fixation – feast or famine? Trends Microbiol 13(9):416–420. https://doi.org/10.1016/j.tim.2005.07.002

    Article  CAS  Google Scholar 

  63. Wasmund N, Voss M, Lochte K (2001) Evidence of nitrogen fixation by non-heterocystous cyanobacteria in the Baltic Sea and re-calculation of a budget of nitrogen fixation. Mar Ecol Prog Ser 214:1–14. https://doi.org/10.3354/meps214001

    Article  CAS  Google Scholar 

  64. Friedman BA, Dugan PR, Pfister RM, Remsen CC (1968) Fine structure and composition of the zoogloeal matrix surrounding Zoogloea ramigera. J Bacteriol 96(6):2144–2153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Suzuki H, Daimon M, Awano T, Umekage S, Tanaka T, Kikuchi Y (2009) Characterization of extracellular DNA production and flocculation of the marine photosynthetic bacterium Rhodovulum sulfidophilum. Appl Microbiol Biotechnol 84:349–356. https://doi.org/10.1007/s00253-009-2031-7

    Article  CAS  PubMed  Google Scholar 

  66. Lupton FS, Marshall KC (1981) Specific adhesion of bacteria to heterocysts of Anabaena spp. and its ecological significance. Appl Environ Microbiol 42(6):1085–1092

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Ji B, Yang K, Zhu L, Jiang Y, Wang H, Zhou J, Zhang H (2015) Aerobic denitrification: a review of important advances of the last 30 years. Biotechnol Bioproc Eng 20(4):643–651

    Article  CAS  Google Scholar 

  68. Degerholm J, Gundersen K, Bergman B, Söderbäck E (2006) Phosphorus-limited growth dynamics in two Baltic Sea cyanobacteria, Nodularia sp. and Aphanizomenon sp. FEMS Microbiol Ecol 58(3):323–332. https://doi.org/10.1111/j.1574-6941.2006.00180.x

    Article  CAS  PubMed  Google Scholar 

  69. Dortch Q (1990) The interaction between ammonium and nitrate uptake in phytoplankton. Mar Ecol Prog Ser 61(1/2):183–201

    Article  CAS  Google Scholar 

  70. Frías JE, Flores E (2015) Induction of the nitrate assimilation nirA operon and protein-protein interactions in the maturation of nitrate and nitrite reductases in the cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 197(14):2442–2452. https://doi.org/10.1128/JB.00198-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Paerl HW, Huisman J (2008) Blooms like it hot. Science 320:57–58. https://doi.org/10.1126/science.1155398

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by the “The role of atmospheric nitrogen fixation in the largest eutrophicated European lagoon (NitFix)” (Agreement No. P-MIP-17-126) grant under agreement with the Research Council of Lithuania (LMTLT). We gratefully thank Adelė Mačiūtė, Akvilė Kančauskaitė, Donata Overlingė, Jolita Petkuvienė, and Irma Vybernaitė-Lubienė for assistance in field sampling and laboratory analysis and Paul A. Bukaveckas for many helpful comments on earlier version of this manuscript. We kindly thank the Editor and two anonymous reviewers for their constructive comments.

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  1. Stefano Bonaglia

    Present address: Department of Marine Sciences, University of Gothenburg, Box 461, 40530 Gothenburg, Sweden

Authors and Affiliations

  1. Marine Research Institute, Klaipeda University, 92294, Klaipeda, Lithuania

    Mindaugas Zilius, Aurelija Samuiloviene & Stefano Bonaglia

  2. Department of Molecular Microbiology and Biotechnology, Institute of Biochemistry, Life Sciences Center, Vilnius University, 10257 Vilnius, Lithuania

    Rūta Stanislauskienė & Rolandas Meškys

  3. Baltic Sea Center, Stockholm University, Stockholm, Sweden

    Elias Broman

  4. Department of Ecology, Environment and Plant Sciences, Stockholm University, 10691 Stockholm, Sweden

    Elias Broman & Stefano Bonaglia

  5. Department of Biology, University of Southern Denmark, 5230, Odense, Denmark

    Stefano Bonaglia

  6. Coastal and Freshwater Group, Cawthron Institute, 7042 Nelson, New Zealand

    Anastasija Zaiko

  7. Institute of Marine Science, University of Auckland, Private Bag 92019, Auckland, New Zealand

    Anastasija Zaiko

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Zilius, M., Samuiloviene, A., Stanislauskienė, R. et al. Depicting Temporal, Functional, and Phylogenetic Patterns in Estuarine Diazotrophic Communities from Environmental DNA and RNA. Microb Ecol 81, 36–51 (2021). https://doi.org/10.1007/s00248-020-01562-1

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