Cyanophage Lysis of the Cyanobacterium Nodularia spumigena Affects the Variability and Fitness of the Host-Associated Microbiome.

Sigitas ��ul��ius, Gediminas Alzbutas, Valiantsin Lukashevich
Author Information
  1. Sigitas ��ul��ius: Laboratory of Algology and Microbial Ecology, Nature Research Centre, Vilnius, Lithuania. ORCID
  2. Gediminas Alzbutas: Laboratory of Algology and Microbial Ecology, Nature Research Centre, Vilnius, Lithuania.
  3. Valiantsin Lukashevich: Laboratory of Algology and Microbial Ecology, Nature Research Centre, Vilnius, Lithuania.

Abstract

Cyanobacteria are intricately linked with its microbiome through multiple metabolic interactions. We assessed how these interactions might be affected by cyanophage infection and lysis in cyanobacterium Nodularia spumigena. The genome-scale metabolic models and analysis of putative metabolic interactions revealed a bidirectional cross-feeding potential within the N. spumigena microbiome, with heterotrophic bacteria exhibiting a greater level of trophic dependency on the cyanobacterium. Our results indicate that microbes associated with N. spumigena rely on the supply of various amino acids, reduced carbon compounds and protein synthesis cofactors released by the cyanobacterial host. We observed that compositional changes in the N. spumigena microbiome were associated with the multiplicity of infection and increased with increasing initial viral load. Higher mortality of N. spumigena led to decreased variability in the relative abundances of bacteria, suggesting an indirect restriction of their niche space. Lysis of N. spumigena resulted in a substantial decline in the estimated absolute abundances of heterotrophic bacteria, indicating reduced fitness of co-occurring bacteria in the absence of N. spumigena. Altogether, we demonstrate how a gradual increase in viral pressure on the photosynthetic host propagates through the co-occurring microbial community, disrupting cooperative nature and microbial connectivity within the N. spumigena microbiome.

Keywords

References

  1. Adam, B., I. Klawonn, and J. B. Sved��n. 2016. ���N2���Fixation, Ammonium Release and N���Transfer to the Microbial and Classical Food Web Within a Plankton Community.��� ISME Journal 10: 450���459. https://doi.org/10.1038/ismej.2015.126.
  2. Ahern, O. M., K. A. Whittaker, T. C. Williams, D. E. Hunt, and T. A. Rynearson. 2021. ���Host Genotype Structures the Microbiome of a Globally Dispersed Marine Phytoplankton.��� Proceedings of the National Academy of Sciences of the United States of America 118: 1���8. https://doi.org/10.1073/pnas.2105207118.
  3. Anders, S., and W. Huber. 2010. ���Differential Expression Analysis for Sequence Count Data.��� Genome Biology 11: R106. https://doi.org/10.1186/gb���2010���11���10���r106.
  4. Ashraf, N., F. Ahmad, and Y. Lu. 2023. ���Synergy Between Microalgae and Microbiome in Polluted Waters.��� Trends in Microbiology 31: 9���21. https://doi.org/10.1016/j.tim.2022.06.004.
  5. Bankevich, A., S. Nurk, and D. Antipov. 2012. ���SPAdes: A New Genome Assembly Algorithm and Its Applications to Single���Cell Sequencing.��� Journal of Computational Biology 19: 455���477. https://doi.org/10.1089/cmb.2012.0021.
  6. Berg, C., C. L. Dupont, and J. Asplund���Samuelsson. 2018. ���Dissection of Microbial Community Functions During a Cyanobacterial Bloom in the Baltic Sea via Metatranscriptomics.��� Frontiers in Marine Science 5: 55. https://doi.org/10.3389/fmars.2018.00055.
  7. Berg, K. a., C. Lyra, K. Sivonen, et al. 2009. ���High Diversity of Cultivable Heterotrophic Bacteria in Association With Cyanobacterial Water Blooms.��� ISME Journal 3: 314���325. https://doi.org/10.1038/ismej.2008.110.
  8. Berga, M., A. J. Sz��kely, and S. Langenheder. 2012. ���Effects of Disturbance Intensity and Frequency on Bacterial Community Composition and Function.��� PLoS One 7: e36959. https://doi.org/10.1371/journal.pone.0036959.
  9. Berngruber, T. W., S. Lion, and S. Gandon. 2013. ���Evolution of Suicide as a Defence Strategy Against Pathogens in a Spatially Structured Environment.��� Ecology Letters 16: 446���453. https://doi.org/10.1111/ele.12064.
  10. Besemer, J., A. Lomsadze, and M. Borodovsky. 2001. ���GeneMarkS: A Self���Training Method for Prediction of Gene Starts in Microbial Genomes. Implications for Finding Sequence Motifs in Regulatory Regions.��� Nucleic Acids Research 29: 2607���2618. https://doi.org/10.1093/nar/29.12.2607.
  11. Bolger, A. M., M. Lohse, and B. Usadel. 2014. ���Trimmomatic: A Flexible Trimmer for Illumina Sequence Data.��� Bioinformatics 30: 2114���2120. https://doi.org/10.1093/bioinformatics/btu170.
  12. Bolhuis, H., I. Severin, V. Confurius���Guns, U. I. A. Wollenzien, and L. J. Stal. 2010. ���Horizontal Transfer of the Nitrogen Fixation Gene Cluster in the Cyanobacterium Microcoleus chthonoplastes.��� ISME Journal 4: 121���130. https://doi.org/10.1038/ismej.2009.99.
  13. Brown, C. M., and K. D. Bidle. 2014. ���Attenuation of Virus Production at High Multiplicities of Infection in Aureococcus Anophagefferens.��� Virology 466���467: 71���81. https://doi.org/10.1016/j.virol.2014.07.023.
  14. Brussaard, C. P. D., A. A. M. Noordeloos, R. A. Sandaa, M. Heldal, and G. Bratbak. 2004. ���Discovery of a dsRNA Virus Infecting the Marine Photosynthetic Protist Micromonas pusilla.��� Virology 319: 280���291. https://doi.org/10.1016/j.virol.2003.10.033.
  15. Brussaard, C. P. D., S. W. Wilhelm, and F. Thingstad. 2008. ���Global���Scale Processes With a Nanoscale Drive: The Role of Marine Viruses.��� ISME Journal 2: 575���578. https://doi.org/10.1038/ismej.2008.31.
  16. Brzezowski, P., A. S. Richter, and B. Grimm. 2015. ���Regulation and Function of Tetrapyrrole Biosynthesis in Plants and Algae.��� Biochimica et Biophysica Acta, Bioenergetics 1847: 968���985. https://doi.org/10.1016/j.bbabio.2015.05.007.
  17. Buchan, A., G. R. LeCleir, C. A. Gulvik, and J. M. Gonzalez. 2014. ���Master Recyclers: Features and Functions of Bacteria Associated With Phytoplankton Blooms.��� Nature Reviews. Microbiology 12: 686���698. https://doi.org/10.1038/nrmicro3326.
  18. Buchfink, B., C. Xie, and D. H. Huson. 2015. ���Fast and Sensitive Protein Alignment Using DIAMOND.��� Nature Methods 12: 59���60. https://doi.org/10.1038/nmeth.3176.
  19. Cai, L., H. Li, J. Deng, R. Zhou, and Q. Zeng. 2024. ���Biological Interactions With Prochlorococcus: Implications for the Marine Carbon Cycle.��� Trends in Microbiology 32: 280���291. https://doi.org/10.1016/j.tim.2023.08.011.
  20. Cairns, J., S. Coloma, K. Sivonen, and T. Hiltunen. 2016. ���Evolving Interactions Between Diazotrophic Cyanobacterium and Phage Mediate Nitrogen Release and Host Competitive Ability.��� Royal Society Open Science 3: 160839. https://doi.org/10.1098/rsos.160839.
  21. Cavaliere, M., S. Feng, O. S. Soyer, and J. I. Jim��nez. 2017. ���Cooperation in Microbial Communities and Their Biotechnological Applications.��� Environmental Microbiology 19: 2949���2963. https://doi.org/10.1111/1462���2920.13767.
  22. Chaumeil, P. A., A. J. Mussig, P. Hugenholtz, and D. H. Parks. 2020. ���GTDB���Tk: A Toolkit to Classify Genomes With the Genome Taxonomy Database.��� Bioinformatics 36: 1925���1927. https://doi.org/10.1093/bioinformatics/btz848.
  23. Cheng, K., T. Frenken, C. P. D. Brussaard, and D. B. van de Waal. 2019. ���Cyanophage Propagation in the Freshwater Cyanobacterium Phormidiumis Constrained by Phosphorus Limitation and Enhanced by Elevated pCO2.��� Frontiers in Microbiology 10: 1���11. https://doi.org/10.3389/fmicb.2019.00617.
  24. Christiansen, R. H., L. Madsen, I. Dalsgaard, D. Castillo, P. G. Kalatzis, and M. Middelboe. 2016. ���Effect of Bacteriophages on the Growth of Flavobacterium Psychrophilum and Development of Phage���Resistant Strains.��� Microbial Ecology 71: 845���859. https://doi.org/10.1007/s00248���016���0737���5.
  25. Cohan, F. M. 1994. ���Genetic Exchange and Evolutionary Divergence in Prokaryotes.��� Trends in Ecology & Evolution 9: 175���180. https://doi.org/10.1016/0169���5347(94)90081���7.
  26. Coloma, S. E., A. Dienstbier, D. H. Bamford, K. Sivonen, E. Roine, and T. Hiltunen. 2017. ���Newly Isolated Nodularia Phage Influences Cyanobacterial Community Dynamics.��� Environmental Microbiology 19: 273���286. https://doi.org/10.1111/1462���2920.13601.
  27. Cook, K. V., C. Li, and H. Cai. 2020. ���The Global Microcystis Interactome.��� Limnology and Oceanography 65: S194���S207. https://doi.org/10.1002/lno.11361.
  28. Curriert, T. C., and C. P. Wolk. 1979. ���Characteristics of Anabaena variabilis Influencing Plaque Formation by Cyanophage N���1.��� Journal of Bacteriology 139: 88���92.
  29. Darling, A. E., B. Mau, and N. T. Perna. 2010. ���Progressivemauve: Multiple Genome Alignment With Gene Gain, Loss and Rearrangement.��� PLoS One 5: e11147. https://doi.org/10.1371/journal.pone.0011147.
  30. De Smet, J., M. Zimmermann, and M. Kogadeeva. 2016. ���High Coverage Metabolomics Analysis Reveals Phage���Specific Alterations to Pseudomonas aeruginosa Physiology During Infection.��� ISME Journal 10: 1823���1835. https://doi.org/10.1038/ismej.2016.3.
  31. Delcher, A. L., D. Harmon, S. Kasif, O. White, and S. L. Salzberg. 1999. ���Improved Microbial Gene Identification With GLIMMER.��� Nucleic Acids Research 27: 4636���4641. https://doi.org/10.1093/nar/27.23.4636.
  32. D'Souza, G., S. Shitut, D. Preussger, G. Yousif, S. Waschina, and C. Kost. 2018. ���Ecology and Evolution of Metabolic Cross���Feeding Interactions in Bacteria.��� Natural Product Reports 35: 455���488. https://doi.org/10.1039/c8np00009c.
  33. Dupuis, S., U. F. Lingappa, X. Mayali, et al. 2024. ���Scarcity of Fixed Carbon Transfer in a Model Microbial Phototroph���Heterotroph Interaction.��� ISME Journal 18: wrae140. https://doi.org/10.1093/ismejo/wrae140.
  34. Eriksen, R. S., N. Mitarai, and K. Sneppen. 2020. ���On Phage Adsorption to Bacterial Chains.��� Biophysical Journal 119: 1896���1904. https://doi.org/10.1016/j.bpj.2020.09.027.
  35. Fang, X., Y. Liu, and Y. Zhao. 2019. ���Transcriptomic Responses of the Marine Cyanobacterium Prochlorococcus to Viral Lysis Products.��� Environmental Microbiology 21: 2015���2028. https://doi.org/10.1111/1462���2920.14513.
  36. Fazzino, L., J. Anisman, J. M. Chac��n, R. H. Heineman, and W. R. Harcombe. 2020. ���Lytic Bacteriophage Have Diverse Indirect Effects in a Synthetic Cross���Feeding Community.��� ISME Journal 14: 123���134. https://doi.org/10.1038/s41396���019���0511���z.
  37. Fernandes, A. D., J. M. Macklaim, T. G. Linn, G. Reid, and G. B. Gloor. 2013. ���ANOVA���Like Differential Expression (ALDEx) Analysis for Mixed Population RNA���Seq.��� PLoS One 8: e67019. https://doi.org/10.1371/journal.pone.0067019.
  38. Flynn, K. J., S. A. Kimmance, D. R. Clark, A. Mitra, L. Polimene, and W. H. Wilson. 2021. ���Modelling the Effects of Traits and Abiotic Factors on Viral Lysis in Phytoplankton.��� Frontiers in Marine Science 8: 1���23. https://doi.org/10.3389/fmars.2021.667184.
  39. Friedman, J., and E. J. Alm. 2012. ���Inferring Correlation Networks From Genomic Survey Data.��� PLoS Computational Biology 8: 1���11. https://doi.org/10.1371/journal.pcbi.1002687.
  40. Frischkorn, K. R., S. T. Haley, and S. T. Dyhrman. 2018. ���Coordinated Gene Expression Between Trichodesmium and Its Microbiome Over Day���Night Cycles in the North Pacific Subtropical Gyre.��� ISME Journal 12: 997���1007. https://doi.org/10.1038/s41396���017���0041���5.
  41. Fritts, R. K., A. L. McCully, and J. B. McKinlay. 2021. ���Extracellular Metabolism Sets the Table for Microbial Cross���Feeding.��� Microbiology and Molecular Biology Reviews 85: e00135���20. https://doi.org/10.1128/mmbr.00135���20.
  42. Guan, J., Y. Chen, Y.���X. Goh, et al. 2024. ���TADB 3.0: An Updated Database of Bacterial Toxin���Antitoxin Loci and Associated Mobile Genetic Elements.��� Nucleic Acids Research 52: D784���D790. https://doi.org/10.1093/nar/gkad962.
  43. Guillard, R. R. L. 1975. ���Culture of Phytoplankton for Feeding Marine Invertebrates.��� In Culture of Marine Invertebrate Animals, edited by W. L. Smith and M. H. Chanley, 29���60. Springer US.
  44. Hewson, I., J. M. O'Neil, C. A. Heil, G. Bratbak, and W. C. Dennison. 2001. ���Effects of Concentrated Viral Communities on Photosynthesis and Community Composition of Co���Occurring Benthic Microalgae and Phytoplankton.��� Aquatic Microbial Ecology 25: 1���10. https://doi.org/10.3354/ame025001.
  45. Howard���Varona, C., M. M. Lindback, and G. E. Bastien. 2020. ���Phage���Specific Metabolic Reprogramming of Virocells.��� ISME Journal 14: 881���895. https://doi.org/10.1038/s41396���019���0580���z.
  46. Isaac, A., A. R. Mohamed, and S. A. Amin. 2024. ���Rhodobacteraceae Are Key Players in Microbiome Assembly of the Diatom Asterionellopsis glacialis.��� Applied and Environmental Microbiology 90: e0057024. https://doi.org/10.1128/aem.00570���24.
  47. Jackson, D. A. 1997. ���Compositional Data in Community Ecology: The Paradigm or Peril of Proportions?��� Ecology 78: 929���940. https://doi.org/10.1890/0012���9658(1997)078[0929:CDICET]2.0.CO;2.
  48. Jover, L. F., T. C. Effler, A. Buchan, S. W. Wilhelm, and J. S. Weitz. 2014. ���The Elemental Composition of Virus Particles: Implications for Marine Biogeochemical Cycles.��� Nature Reviews. Microbiology 12: 519���528. https://doi.org/10.1038/nrmicro3289.
  49. Kai, C., S. S. Yu, G. Ying, Z. Y. Jun, and H. Z. Guang. 2015. ���Long���Term Effects of Elevated CO2 on the Proliferation of Cyanophage PP.��� Open Biotechnology Journal 9: 100���103.
  50. Karjalainen, M., J. Engstr��m�����st, S. Korpinen, et al. 2007. ���Ecosystem Consequences of Cyanobacteria in the Northern Baltic Sea.��� Ambio 36: 195���202. https://doi.org/10.1579/0044���7447(2007)36[195:ECOCIT]2.0.CO;2.
  51. Kimura, S., Y. Sako, and T. Yoshida. 2013. ���Rapid Microcystis Cyanophage Gene Diversification Revealed by Longand Short���Term Genetic Analyses of the Tail Sheath Gene in a Natural Pond.��� Applied and Environmental Microbiology 79: 2789���2795. https://doi.org/10.1128/AEM.03751���12.
  52. Kimura���Sakai, S., Y. Sako, and T. Yoshida. 2015. ���Development of a Real���Time PCR Assay for the Quantification of Ma���LMM01���Type Microcystis Cyanophages in a Natural Pond.��� Letters in Applied Microbiology 60: 400���408. https://doi.org/10.1111/lam.12387.
  53. Klawonn, I., N. Nahar, and J. Walve. 2016. ���Cell���Specific Nitrogen��� and Carbon���Fixation of Cyanobacteria in a Temperate Marine System (Baltic Sea).��� Environmental Microbiology 18: 4596���4609. https://doi.org/10.1111/1462���2920.13557.
  54. Klopfenstein, D. V., L. Zhang, and B. S. Pedersen. 2018. ���GOATOOLS: A Python Library for Gene Ontology Analyses.��� Scientific Reports 8: 1���17. https://doi.org/10.1038/s41598���018���28948���z.
  55. Kust, A., J. Zorz, C. C. Paniker, et al. 2023. ���Model Cyanobacterial Consortia Reveal a Consistent Core Microbiome Independent of Inoculation Source or Cyanobacterial Host Species.��� bioRxiv: 1���33. https://doi.org/10.1101/2023.12.09.570939.
  56. Kuznecova, J., S. ��ul��ius, A. Vogts, M. Voss, K. J��rgens, and E. ��imoli��nas. 2020. ���Nitrogen Flow in Diazotrophic Cyanobacterium Aphanizomenon Flos���Aquae Is Altered by Cyanophage Infection.��� Frontiers in Microbiology 11: 1���14. https://doi.org/10.3389/fmicb.2020.02010.
  57. Langenheder, S., M. Berga, ��. ��stman, and A. J. Sz��kely. 2012. ���Temporal Variation of �����Diversity and Assembly Mechanisms in a Bacterial Metacommunity.��� ISME Journal 6: 1107���1114. https://doi.org/10.1038/ismej.2011.177.
  58. Lehtim��ki, J., K. Sivonen, R. Luukkainen, and S. I. Niemel��. 1994. ���The Effects of Incubation Time, Temperature, Light, Salinity, and Phosphorus on Growth and Hepatotoxin Production by Nodularia Strains.��� Archiv f��r Hydrobiologie 130: 269���282. https://doi.org/10.1127/archiv���hydrobiol/130/1994/269.
  59. Li, H. 2018. ���Minimap2: Pairwise Alignment for Nucleotide Sequences.��� Bioinformatics 34: 3094���3100. https://doi.org/10.1093/bioinformatics/bty191.
  60. Liu, L., Y. Yang, Y. Deng, and T. Zhang. 2022. ���Nanopore Long���Read���Only Metagenomics Enables Complete and High���Quality Genome Reconstruction From Mock and Complex Metagenomes.��� Microbiome 10: 209. https://doi.org/10.1186/s40168���022���01415���8.
  61. Louca, S., and M. Doebeli. 2017. ���Taxonomic Variability and Functional Stability in Microbial Communities Infected by Phages.��� Environmental Microbiology 19: 3863���3878. https://doi.org/10.1111/1462���2920.13743.
  62. Ma, X., M. L. Coleman, and J. R. Waldbauer. 2018. ���Distinct Molecular Signatures in Dissolved Organic Matter Produced by Viral Lysis of Marine Cyanobacteria.��� Environmental Microbiology 20: 3001���3011. https://doi.org/10.1111/1462���2920.14338.
  63. Mandal, S., W. van Treuren, R. A. White, M. Eggesb��, R. Knight, and S. D. Peddada. 2015. ���Analysis of Composition of Microbiomes: A Novel Method for Studying Microbial Composition.��� Microbial Ecology in Health and Disease 26: 1371. https://doi.org/10.3402/mehd.v26.27663.
  64. Mars Brisbin, M., S. Mitarai, M. A. Saito, and H. Alexander. 2022. ���Microbiomes of Bloom���Forming Phaeocystis Algae Are Stable and Consistently Recruited, With Both Symbiotic and Opportunistic Modes.��� ISME Journal 16: 2255���2264. https://doi.org/10.1038/s41396���022���01263���2.
  65. Martin, R. M., M. Moniruzzaman, and N. C. Mucci. 2019. ���Cylindrospermopsis raciborskii Virus and Host: Genomic Characterization and Ecological Relevance.��� Environmental Microbiology 21: 1942���1956. https://doi.org/10.1111/1462���2920.14425.
  66. Mayo���Mu��oz, D., R. Pinilla���Redondo, N. Birkholz, and P. C. Fineran. 2023. ���A Host of Armor: Prokaryotic Immune Strategies Against Mobile Genetic Elements.��� Cell Reports 42: 38���43. https://doi.org/10.1016/j.celrep.2023.112672.
  67. Mehnert, G., J. Rucker, and C. Wiedner. 2014. ���Population Dynamics and Akinete Formation of an Invasive and a Native Cyanobacterium in Temperate Lakes.��� Journal of Plankton Research 36: 378���387. https://doi.org/10.1093/plankt/fbt122.
  68. Millman, A., S. Melamed, and A. Leavitt. 2022. ���An Expanded Arsenal of Immune Systems That Protect Bacteria From Phages.��� Cell Host & Microbe 30: 1556���1569. https://doi.org/10.1016/j.chom.2022.09.017.
  69. M��lder, F., K. P. Jablonski, and B. Letcher. 2021. ���Sustainable Data Analysis with Snakemake.��� F1000Research 10: 33. https://doi.org/10.12688/f1000research.29032.2.
  70. Morimoto, D., S. ��ul��ius, K. Tominaga, and T. Yoshida. 2020a. ���Predetermined Clockwork Microbial Worlds: Current Understanding of Aquatic Microbial Diel Response From Model Systems to Complex Environments.��� In Advances in Applied Microbiology, 163���191. Elsevier.
  71. Morimoto, D., S. ��ul��ius, and T. Yoshida. 2020b. ���Viruses of Freshwater Bloom���Forming Cyanobacteria: Genomic Features, Infection Strategies and Coexistence With the Host.��� Environmental Microbiology Reports 12: 486���502. https://doi.org/10.1111/1758���2229.12872.
  72. Morimoto, D., K. Tominaga, H. Takebe, S. ��ul��ius, and T. Yoshida. 2022. ���Viral Nature of the Aquatic Ecosystems.��� In The Biological Role of a Virus, edited by C. J. Hurst, 3���25. Springer Nature Switzerland.
  73. Morton, J. T., C. Marotz, A. Washburne, et al. 2019. ���Establishing Microbial Composition Measurement Standards With Reference Frames.��� Nature Communications 10: 2719. https://doi.org/10.1038/s41467���019���10656���5.
  74. Motwani, N. H., J. Duberg, J. B. Sved��n, and E. Gorokhova. 2018. ���Grazing on Cyanobacteria and Transfer of Diazotrophic Nitrogen to Zooplankton in the Baltic Sea.��� Limnology and Oceanography 63: 672���686. https://doi.org/10.1002/lno.10659.
  75. Nayfach, S., A. P. Camargo, F. Schulz, E. Eloe���Fadrosh, S. Roux, and N. C. Kyrpides. 2021. ���CheckV Assesses the Quality and Completeness of Metagenome���Assembled Viral Genomes.��� Nature Biotechnology 39: 578���585. https://doi.org/10.1038/s41587���020���00774���7.
  76. Nearing, J. T., G. M. Douglas, and M. G. Hayes. 2022. ���Microbiome Differential Abundance Methods Produce Different Results Across 38 Datasets.��� Nature Communications 13: 1���16. https://doi.org/10.1038/s41467���022���28034���z.
  77. Nishimura, Y., T. Yoshida, M. Kuronishi, H. Uehara, H. Ogata, and S. Goto. 2017. ���ViPTree: The Viral Proteomic Tree Server.��� Bioinformatics 33: 2379���2380. https://doi.org/10.1093/bioinformatics/btx157.
  78. Olofsson, M., J. Egardt, A. Singh, and H. Ploug. 2016. ���Inorganic Phosphorus Enrichments in Baltic Sea Water Have Large Effects on Growth, Carbon Fixation, and N2 Fixation by Nodularia spumigena.��� Aquatic Microbial Ecology 77: 111���123. https://doi.org/10.3354/ame01795.
  79. Padan, E., and M. Shilo. 1973. ���Cyanophages���Viruses Attacking Blue���Green Algae.��� Bacteriological Reviews 37: 343���370. https://doi.org/10.1128/br.37.3.343���370.1973.
  80. Parks, D. H., M. Imelfort, C. T. Skennerton, P. Hugenholtz, and G. W. Tyson. 2015. ���CheckM: Assessing the Quality of Microbial Genomes Recovered From Isolates, Single Cells, and Metagenomes.��� Genome Research 25: 1043���1055. https://doi.org/10.1101/gr.186072.114.
  81. P��rez���Carrascal, O. M., N. Tromas, Y. Terrat, et al. 2021. ���Single���Colony Sequencing Reveals Microbe���By���Microbiome Phylosymbiosis Between the Cyanobacterium Microcystis and Its Associated Bacteria.��� Microbiome 9: 1���21. https://doi.org/10.1186/s40168���021���01140���8.
  82. Piwosz, K., T. Shabarova, J. Pernthaler, et al. 2020. ���Bacterial and Eukaryotic Small���Subunit Amplicon Data Do Not Provide a Quantitative Picture of Microbial Communities, but They Are Reliable in the Context of Ecological Interpretations.��� mSphere 5, no. 2: e00052���20. https://doi.org/10.1128/msphere.00052���20.
  83. Ploug, H., B. Adam, N. Musat, et al. 2011. ���Carbon, Nitrogen and O2 Fluxes Associated With the Cyanobacterium Nodularia spumigena in the Baltic Sea.��� ISME Journal 5: 1549���1558. https://doi.org/10.1038/ismej.2011.20.
  84. Popa, O., and T. Dagan. 2011. ���Trends and Barriers to Lateral Gene Transfer in Prokaryotes.��� Current Opinion in Microbiology 14: 615���623. https://doi.org/10.1016/j.mib.2011.07.027.
  85. Props, R., F. M. Kerckhof, and P. Rubbens. 2017. ���Absolute Quantification of Microbial Taxon Abundances.��� ISME Journal 11: 584���587. https://doi.org/10.1038/ismej.2016.117.
  86. Quinn, T. P., T. M. Crowley, and M. F. Richardson. 2018. ���Benchmarking Differential Expression Analysis Tools for RNA���Seq: Normalization���Based vs. Log���Ratio Transformation���Based Methods.��� BMC Bioinformatics 19: 1���15. https://doi.org/10.1186/s12859���018���2261���8.
  87. Rawat, P., S. Das, D. Shankhdhar, and S. C. Shankhdhar. 2021. ���Phosphate���Solubilizing Microorganisms: Mechanism and Their Role in Phosphate Solubilization and Uptake.��� Journal of Soil Science and Plant Nutrition 21: 49���68. https://doi.org/10.1007/s42729���020���00342���7.
  88. Roager, L., P. J. Kempen, M. Bentzon���Tilia, E. C. Sonnenschein, and L. Gram. 2023. ���Impact of Host Species on Assembly, Composition, and Functional Profiles of Phycosphere Microbiomes.��� mSystems 9: 1���19.
  89. Russel, J., R. Pinilla���Redondo, D. Mayo���Mu��oz, S. A. Shah, and S. J. S��rensen. 2020. ���CRISPRCasTyper: Automated Identification, Annotation, and Classification of CRISPR���Cas Loci.��� CRISPR Journal 3: 462���469. https://doi.org/10.1089/crispr.2020.0059.
  90. Sarmento, H., C. Morana, and J. M. Gasol. 2016. ���Bacterioplankton Niche Partitioning in the Use of Phytoplankton���Derived Dissolved Organic Carbon: Quantity Is More Important Than Quality.��� ISME Journal 10: 2582���2592. https://doi.org/10.1038/ismej.2016.66.
  91. Schwalbach, M. S., I. Hewson, and J. A. Fuhrman. 2004. ���Viral Effects on Bacterial Community Composition in Marine Plankton Microcosms.��� Aquatic Microbial Ecology 34: 117���127.
  92. Seemann, T. 2014. ���Prokka: Rapid Prokaryotic Genome Annotation.��� Bioinformatics 30: 2068���2069. https://doi.org/10.1093/bioinformatics/btu153.
  93. Sep��lveda Cisternas, I., J. C. Salazar, and V. A. Garc��a���Angulo. 2018. ���Overview on the Bacterial Iron���Riboflavin Metabolic Axis.��� Frontiers in Microbiology 9: 1���7. https://doi.org/10.3389/fmicb.2018.01478.
  94. Shelford, E. J., M. Middelboe, E. F. M��ller, and C. A. Suttle. 2012. ���Virus���Driven Nitrogen Cycling Enhances Phytoplankton Growth.��� Aquatic Microbial Ecology 66: 41���46. https://doi.org/10.3354/ame01553.
  95. Shelford, E. J., and C. A. Suttle. 2018. ���Virus���Mediated Transfer of Nitrogen From Heterotrophic Bacteria to Phytoplankton.��� Biogeosciences 15: 809���819. https://doi.org/10.5194/bg���15���809���2018.
  96. Simis, S. G. H., M. Tijdens, H. L. Hoogveld, and H. J. Gons. 2005. ���Optical Changes Associated With Cyanobacterial Bloom Termination by Viral Lysis.��� Journal of Plankton Research 27, no. 9: 937���949. https://doi.org/10.1093/plankt/fbi068.
  97. Soucy, S. M., J. Huang, and J. P. Gogarten. 2015. ���Horizontal Gene Transfer: Building the Web of Life.��� Nature Reviews. Genetics 16: 472���482. https://doi.org/10.1038/nrg3962.
  98. Steffen, M. M., B. S. Belisle, S. B. Watson, G. L. Boyer, R. A. Bourbonniere, and S. W. Wilhelm. 2015. ���Metatranscriptomic Evidence for Co���Occurring Top���Down and Bottom���Up Controls on Toxic Cyanobacterial Communities.��� Applied and Environmental Microbiology 81: 3268���3276. https://doi.org/10.1128/AEM.04101���14.
  99. Steffen, M. M., T. W. Davis, and R. M. L. McKay. 2017. ���Ecophysiological Examination of the Lake Erie Microcystis Bloom in 2014: Linkages Between Biology and the Water Supply Shutdown of Toledo, OH.��� Environmental Science & Technology 51: 6745���6755. https://doi.org/10.1021/acs.est.7b00856.
  100. Stevenson, B. S., and J. B. Waterbury. 2006. ���Isolation and Identification of an Epibiotic Bacterium Associated With Heterocystous Anabaena Cells.��� Biological Bulletin 210: 73���77.
  101. ��ul��ius, S., H. Mazur���Marzec, I. Vitonyt��, et al. 2018. ���Insights Into Cyanophage���Mediated Dynamics of Nodularin and Other Non���Ribosomal Peptides in Nodularia spumigena.��� Harmful Algae 78: 69���74. https://doi.org/10.1016/j.hal.2018.07.004.
  102. ��ul��ius, S., K. Slavuckyt��, and R. Pa��kauskas. 2017. ���The Predation Paradox: Synergistic and Antagonistic Interactions Between Grazing by Crustacean Predator and Infection by Cyanophages Promotes Bloom Formation in Filamentous Cyanobacteria.��� Limnology and Oceanography 62: 2189���2199. https://doi.org/10.1002/lno.10559.
  103. Suttle, C. A., and A. M. Chan. 1993. ���Marine Cyanophages Infecting Oceanic and Coastal Strains of Synechococcus: Abundance, Morphology, Cross���Infectivity and Growth Characteristics.��� Marine Ecology Progress Series 92: 99���109. https://doi.org/10.3354/meps092099.
  104. Teikari, J. E., S. Hou, M. Wahlsten, W. R. Hess, and K. Sivonen. 2018. ���Comparative Genomics of the Baltic Sea Toxic Cyanobacteria Nodularia spumigena UHCC 0039 and Its Response to Varying Salinity.��� Frontiers in Microbiology 9: 1���13. https://doi.org/10.3389/fmicb.2018.00356.
  105. Tesson, F., A. Herv��, E. Mordret, et al. 2022. ���Systematic and Quantitative View of the Antiviral Arsenal of Prokaryotes.��� Nature Communications 13, no. 1: 2561. https://doi.org/10.1038/s41467���022���30269���9.
  106. Tesson, F., R. Planel, and A. Egorov. 2024. ���A Comprehensive Resource for Exploring Antiphage Defense: DefenseFinder Webservice, Wiki and Databases.��� Peer Community Journal 4: e91. https://doi.org/10.1101/2024.01.25.577194.
  107. Teurlincx, S., M. Velthuis, D. Seroka, et al. 2017. ���Species Sorting and Stoichiometric Plasticity Control Community C:P Ratio of First���Order Aquatic Consumers P. Jeyasingh [Ed].��� Ecology Letters 20: 751���760. https://doi.org/10.1111/ele.12773.
  108. Thyrhaug, R., A. Larsen, T. F. Thingstad, and G. Bratbak. 2003. ���Stable Coexistence in Marine Algal Host���Virus Systems.��� Marine Ecology Progress Series 254: 27���35. https://doi.org/10.3354/meps254027.
  109. Tkacz, A., M. Hortala, and P. S. Poole. 2018. ���Absolute Quantitation of Microbiota Abundance in Environmental Samples.��� Microbiome 6: 1���13. https://doi.org/10.1186/s40168���018���0491���7.
  110. T��r��nen, P., A. Medlar, and L. Holm. 2018. ���PANNZER2: A Rapid Functional Annotation Web Server.��� Nucleic Acids Research 46: W84���W88. https://doi.org/10.1093/nar/gky350.
  111. Tuomainen, J., S. Hietanen, J. Kuparinen, P. J. Martikainen, and K. Servomaa. 2006. ���Community Structure of the Bacteria Associated With Nodularia Sp. (Cyanobacteria) Aggregates in the Baltic Sea.��� Microbial Ecology 52: 513���522. https://doi.org/10.1007/s00248���006���9130���0.
  112. Vahtera, E., M. Laamanen, and J. M. Rintala. 2007. ���Use of Different Phosphorus Sources by the Bloom���Forming Cyanobacteria Aphanizomenon Flos���Aquae and Nodularia spumigena.��� Aquatic Microbial Ecology 46: 225���237. https://doi.org/10.3354/ame046225.
  113. van Wichelen, J., P. Vanormelingen, G. A. Codd, and W. Vyverman. 2016. ���The Common Bloom���Forming Cyanobacterium Microcystis Is Prone to a Wide Array of Microbial Antagonists.��� Harmful Algae 55: 97���111. https://doi.org/10.1016/j.hal.2016.02.009.
  114. Vandeputte, D., G. Kathagen, and K. D'Hoe. 2017. ���Quantitative Microbiome Profiling Links Gut Community Variation to Microbial Load.��� Nature 551: 507���511. https://doi.org/10.1038/nature24460.
  115. V��zquez���Mart��nez, G., M. H. Rodriguez, F. Hern��ndez���Hern��ndez, and J. E. Ibarra. 2004. ���Strategy to Obtain Axenic Cultures From Field���Collected Samples of the Cyanobacterium Phormidium Animalis.��� Journal of Microbiological Methods 57: 115���121. https://doi.org/10.1016/j.mimet.2003.12.003.
  116. Vo��, B., H. Bolhuis, and D. P. Fewer. 2013. ���Insights Into the Physiology and Ecology of the Brackish���Water���Adapted Cyanobacterium Nodularia spumigena CCY9414 Based on a Genome���Transcriptome Analysis.��� PLoS One 8: 1���22. https://doi.org/10.1371/journal.pone.0060224.
  117. Wang, Z., Q. Chen, J. Zhang, T. Guan, Y. Chen, and W. Shi. 2020. ���Critical Roles of Cyanobacteria as Reservoir and Source for Antibiotic Resistance Genes.��� Environment International 144: 106034. https://doi.org/10.1016/j.envint.2020.106034.
  118. Watkins, S. C., J. R. Smith, P. K. Hayes, and J. E. M. Watts. 2014. ���Characterisation of Host Growth After Infection With a Broad���Range Freshwater Cyanopodophage.��� PLoS One 9: 1���8. https://doi.org/10.1371/journal.pone.0087339.
  119. Weitz, J. S., C. A. Stock, and S. W. Wilhelm. 2015. ���A Multitrophic Model to Quantify the Effects of Marine Viruses on Microbial Food Webs and Ecosystem Processes.��� ISME Journal 9: 1352���1364. https://doi.org/10.1038/ismej.2014.220.
  120. Weitz, J. S., and S. W. Wilhelm. 2012. ���Ocean Viruses and Their Effects on Microbial Communities and Biogeochemical Cycles.��� F1000 Biology Reports 4: 2���9. https://doi.org/10.3410/B4���17.
  121. Wilson, W. H., N. G. Carr, and N. H. Mann. 1996. ���The Effect of Phosphate Status on the Kinetics of Cyanophage Infection in the Oceanic Cyanobacterium Synechococcus Sp. Wh78031.��� Journal of Phycology 32: 506���516. https://doi.org/10.1111/j.0022���3646.1996.00506.x.
  122. Wishart, D. S., S. Han, S. Saha, et al. 2023. ���PHASTEST: Faster Than PHASTER, Better Than PHAST.��� Nucleic Acids Research 51: W443���W450. https://doi.org/10.1093/nar/gkad382.
  123. Woodhouse, J. N., A. S. Kinsela, R. N. Collins, et al. 2016. ���Microbial Communities Reflect Temporal Changes in Cyanobacterial Composition in a Shallow Ephemeral Freshwater Lake.��� ISME Journal 10: 1337���1351. https://doi.org/10.1038/ismej.2015.218.
  124. Yang, L., and J. Chen. 2022. ���A Comprehensive Evaluation of Microbial Differential Abundance Analysis Methods: Current Status and Potential Solutions.��� Microbiome 10: 1���23. https://doi.org/10.1186/s40168���022���01320���0.
  125. Yoshida, T., Y. Takashima, Y. Tomaru, et al. 2006. ���Isolation and Characterization of a Cyanophage Infecting the Toxic Cyanobacterium Microcystis aeruginosa.��� Applied and Environmental Microbiology 72: 1239���1247. https://doi.org/10.1128/AEM.72.2.1239���1247.2006.
  126. Zelezniak, A., S. Andrejev, O. Ponomarova, D. R. Mende, P. Bork, and K. R. Patil. 2015. ���Metabolic Dependencies Drive Species Co���Occurrence in Diverse Microbial Communities.��� Proceedings of the National Academy of Sciences of the United States of America 112: 6449���6454. https://doi.org/10.1073/pnas.1421834112.
  127. Zhang, T., H. Tamman, and K. Coppieters't Wallant. 2022. ���Direct Activation of a Bacterial Innate Immune System by a Viral Capsid Protein.��� Nature 612: 132���140. https://doi.org/10.1038/s41586���022���05444���z.
  128. Zhang, Z., Y. Qu, and S. Li. 2017. ���Soil Bacterial Quantification Approaches Coupling With Relative Abundances Reflecting the Changes of Taxa.��� Scientific Reports 7: 1���11. https://doi.org/10.1038/s41598���017���05260���w.
  129. Zhao, L., L. Z. Lin, and Y. Zeng. 2023. ���The Facilitating Role of Phycospheric Heterotrophic Bacteria in Cyanobacterial Phosphonate Availability and Microcystis Bloom Maintenance.��� Microbiome 11: 1���16. https://doi.org/10.1186/s40168���023���01582���2.
  130. Zhao, Z., M. Gonsior, P. Schmitt���Kopplin, et al. 2019. ���Microbial Transformation of Virus���Induced Dissolved Organic Matter From Picocyanobacteria: Coupling of Bacterial Diversity and DOM Chemodiversity.��� ISME Journal 13: 2551���2565. https://doi.org/10.1038/s41396���019���0449���1.
  131. Zheng, Q., W. Lin, and Y. Wang. 2021. ���Highly Enriched N���Containing Organic Molecules of Synechococcus Lysates and Their Rapid Transformation by Heterotrophic Bacteria.��� Limnology and Oceanography 66: 335���348. https://doi.org/10.1002/lno.11608.
  132. Zheng, X., Y. Wang, T. Yang, Z. He, and Q. Yan. 2020. ���Size���Fractioned Aggregates Within Phycosphere Define Functional Bacterial Communities Related to Microcystis Aeruginosa and Euglena sanguinea Blooms.��� Aquatic Ecology 54: 609���623. https://doi.org/10.1007/s10452���020���09762���0.
  133. Zhou, C., H. Wang, H. Zhao, and T. Wang. 2022. ���FastANCOM: A Fast Method for Analysis of Compositions of Microbiomes.��� Bioinformatics 38: 2039���2041. https://doi.org/10.1093/bioinformatics/btac060.
  134. Zhu, Q., M. Kosoy, and K. Dittmar. 2014. ���HGTector: An Automated Method Facilitating Genome���Wide Discovery of Putative Horizontal Gene Transfers.��� BMC Genomics 15: 717. https://doi.org/10.1186/1471���2164���15���717.
  135. Zimmerman, A. E., C. Howard���Varona, D. M. Needham, et al. 2020. ���Metabolic and Biogeochemical Consequences of Viral Infection in Aquatic Ecosystems.��� Nature Reviews. Microbiology 18: 21���34. https://doi.org/10.1038/s41579���019���0270���x.
  136. Zimmermann, J., C. Kaleta, and S. Waschina. 2021. ���Gapseq: Informed Prediction of Bacterial Metabolic Pathways and Reconstruction of Accurate Metabolic Models.��� Genome Biology 22: 1���35. https://doi.org/10.1186/s13059���021���02295���1.

Grants

  1. S-LL-21-10/Lietuvos Mokslo Taryba

MeSH Term

Microbiota
Bacteriophages
Nodularia
Bacteriolysis
Viral Load
Cyanobacteria

Word Cloud

Created with Highcharts 10.0.0spumigenaNmicrobiomebacteriametabolicinteractionsNodulariamicrobialinfectioncyanobacteriumwithinheterotrophicassociatedreducedhostviralabundancesLysisco-occurringCyanophageecologyCyanobacteriaintricatelylinkedmultipleassessedmightaffectedcyanophagelysisgenome-scalemodelsanalysisputativerevealedbidirectionalcross-feedingpotentialexhibitinggreaterleveltrophicdependencyresultsindicatemicrobesrelysupplyvariousaminoacidscarboncompoundsproteinsynthesiscofactorsreleasedcyanobacterialobservedcompositionalchangesmultiplicityincreasedincreasinginitialloadHighermortalityleddecreasedvariabilityrelativesuggestingindirectrestrictionnichespaceresultedsubstantialdeclineestimatedabsoluteindicatingfitnessabsenceAltogetherdemonstrategradualincreasepressurephotosyntheticpropagatescommunitydisruptingcooperativenatureconnectivityCyanobacteriumAffectsVariabilityFitnessHost-AssociatedMicrobiomeBalticSeaaquaticvirusharmfulalgalblooms

Similar Articles

Cited By