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Rhythmicity of coastal marine picoeukaryotes, bacteria and archaea despite irregular environmental perturbations

The ISME Journal (2018) | Download Citation


Seasonality in marine microorganisms has been classically observed in phytoplankton blooms, and more recently studied at the community level in prokaryotes, but rarely investigated at the scale of individual microbial taxa. Here we test if specific marine eukaryotic phytoplankton, bacterial and archaeal taxa display yearly rhythms at a coastal site impacted by irregular environmental perturbations. Our seven-year study in the Bay of Banyuls (North Western Mediterranean Sea) shows that despite some fluctuating environmental conditions, many microbial taxa displayed significant yearly rhythms. The robust rhythmicity was found in both autotrophs (picoeukaryotes and cyanobacteria) and heterotrophic prokaryotes. Sporadic meteorological events and irregular nutrient supplies did, however, trigger the appearance of less common non-rhythmic taxa. Among the environmental parameters that were measured, the main drivers of rhythmicity were temperature and day length. Seasonal autotrophs may thus be setting the pace for rhythmic heterotrophs. Similar environmental niches may be driving seasonality as well. The observed strong association between Micromonas and SAR11, which both need thiamine precursors for growth, could be a first indication that shared nutritional niches may explain some rhythmic patterns of co-occurrence.

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  1. 1.

    Antle MC, Silver R. Circadian insights into motivated behavior. In: Simpson EH, Balsam PD, (eds). Behavioral neuroscience of motivation . Cham: Springer International Publishing; 2015. p. 137–69.

  2. 2.

    MacDonald CC, McMahon KW. The flowers that bloom in the spring: RNA processing and seasonal flowering. Cell. 2003;113:671–72.

  3. 3.

    Treusch AH, Demir-Hilton E, Vergin KL, Worden AZ, Carlson CA, Donatz MG, et al. Phytoplankton distribution patterns in the northwestern Sargasso Sea revealed by small subunit rRNA genes from plastids. ISME J. 2012;6:481–92.

  4. 4.

    Sverdrup HU. On vernal blooming of phytoplankton. J Cons Exp Mer. 1953;18:287–95.

  5. 5.

    Behrenfeld MJ. Abandoning Sverdrup’s critical depth hypothesis on phytoplankton blooms. Ecology. 2010;91:977–989.

  6. 6.

    Fowler S, Lee K, Onouchi H, Samach A, Richardson K, Morris B, et al. GIGANTEA: a circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. EMBO J. 1999;18:4679–88.

  7. 7.

    Cohen SE, Golden SS. Circadian rhythms in Cyanobacteria. Microbiol Mol Biol Rev. 2015;79:373–85.

  8. 8.

    Corellou F, Schwartz C, Motta J-P, Djouani-Tahri EB, Sanchez F, Bouget F-Y. Clocks in the green lineage: comparative functional analysis of the circadian architecture of the picoeukaryote ostreococcus. Plant Cell. 2009;21:3436–49.

  9. 9.

    Edmunds L, Adams K. Clocked cell cycle clocks. Science. 1981;211:1002–13.

  10. 10.

    Jacquet S, Partensky F, Lennon J-F, Vaulot D. Diel patterns of growth and division in marine picoplankton in culture. J Phycol. 2001;37:357–69.

  11. 11.

    Alonso-Sáez L, Balagué V, Sá EL, Sánchez O, González JM, Pinhassi J, et al. Seasonality in bacterial diversity in north-west Mediterranean coastal waters: assessment through clone libraries, fingerprinting and FISH: Seasonality in marine bacterial diversity. FEMS Microbiol Ecol. 2007;60:98–112.

  12. 12.

    Chow C-ET, Sachdeva R, Cram JA, Steele JA, Needham DM, Patel A, et al. Temporal variability and coherence of euphotic zone bacterial communities over a decade in the Southern California Bight. ISME J. 2013;7:2259–73.

  13. 13.

    Cram JA, Chow C-ET, Sachdeva R, Needham DM, Parada AE, Steele JA, et al. Seasonal and interannual variability of the marine bacterioplankton community throughout the water column over ten years. ISME J. 2015;9:563–80.

  14. 14.

    Gilbert JA, Steele JA, Caporaso JG, Steinbrück L, Reeder J, Temperton B, et al. Defining seasonal marine microbial community dynamics. ISME J. 2012;6:298–308.

  15. 15.

    Salter I, Galand PE, Fagervold SK, Lebaron P, Obernosterer I, Oliver MJ, et al. Seasonal dynamics of active SAR11 ecotypes in the oligotrophic Northwest Mediterranean Sea. ISME J. 2015;9:347–60.

  16. 16.

    Tonkin JD, Bogan MT, Bonada N, Rios-Touma B, Lytle DA. Seasonality and predictability shape temporal species diversity. Ecology. 2017;98:1201–16.

  17. 17.

    Ladau J, Sharpton TJ, Finucane MM, Jospin G, Kembel SW, O’Dwyer J, et al. Global marine bacterial diversity peaks at high latitudes in winter. Isme J. 2013;7:1669.

  18. 18.

    Bunse C, Pinhassi J. Marine bacterioplankton seasonal succession dynamics. Trends Microbiol. 2017;25:494–505.

  19. 19.

    Fuhrman JA, Cram JA, Needham DM. Marine microbial community dynamics and their ecological interpretation. Nat Rev Microbiol. 2015;13:133–146.

  20. 20.

    Galand PE, Gutiérrez-Provecho C, Massana R, Gasol JM, Casamayor EO. Inter-annual recurrence of archaeal assemblages in the coastal NW Mediterranean Sea (Blanes Bay Microbial Observatory). Limnol Oceanogr. 2010;55:2117–25.

  21. 21.

    Lindh MV, Sjöstedt J, Andersson AF, Baltar F, Hugerth LW, Lundin D, et al. Disentangling seasonal bacterioplankton population dynamics by high-frequency sampling: high-resolution temporal dynamics of marine bacteria. Environ Microbiol. 2015;17:2459–76.

  22. 22.

    Treusch AH, Vergin KL, Finlay LA, Donatz MG, Burton RM, Carlson CA, et al. Seasonality and vertical structure of microbial communities in an ocean gyre. ISME J. 2009;3:1148–63.

  23. 23.

    Vergin KL, Beszteri B, Monier A, Cameron Thrash J, Temperton B, Treusch AH, et al. High-resolution SAR11 ecotype dynamics at the Bermuda Atlantic Time-series study site by phylogenetic placement of pyrosequences. ISME J. 2013;7:1322–32.

  24. 24.

    Fuhrman JA, Hewson I, Schwalbach MS, Steele JA, Brown MV, Naeem S. Annually reoccurring bacterial communities are predictable from ocean conditions. Proc Natl Acad Sci USA. 2006;103:13104–09.

  25. 25.

    Hugoni M, Taib N, Debroas D, Domaizon I, Jouan Dufournel I, Bronner G, et al. Structure of the rare archaeal biosphere and seasonal dynamics of active ecotypes in surface coastal waters. Proc Natl Acad Sci USA. 2013;110:6004–9.

  26. 26.

    Winder M, Cloern JE. The annual cycles of phytoplankton biomass. Philos Trans R Soc B: Biol Sci. 2010;365:3215–26.

  27. 27.

    Brannock PM, Ortmann AC, Moss AG, Halanych KM. Metabarcoding reveals environmental factors influencing spatio‐temporal variation in pelagic micro‐eukaryotes. Mol Ecol. 2016;25:3593–604.

  28. 28.

    Kim DY, Countway PD, Jones AC, Schnetzer A, Yamashita W, Tung C, et al. Monthly to interannual variability of microbial eukaryote assemblages at four depths in the eastern North Pacific. ISME J. 2014;8:515–30.

  29. 29.

    Steele JA, Countway PD, Xia L, Vigil PD, Beman JM, Kim DY, et al. Marine bacterial, archaeal and protistan association networks reveal ecological linkages. ISME J. 2011;5:1414–25.

  30. 30.

    Needham DM, Fuhrman JA. Pronounced daily succession of phytoplankton, archaea and bacteria following a spring bloom. Nat Microbiol. 2016;1:16005.

  31. 31.

    Parada AE, Needham DM, Fuhrman JA. Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environ Microbiol. 2016;18:1403–14.

  32. 32.

    Mangot J-F, Domaizon I, Taib N, Marouni N, Duffaud E, Bronner G, et al. Short-term dynamics of diversity patterns: evidence of continual reassembly within lacustrine small eukaryotes: short-term dynamics of small eukaryotes. Environ Microbiol. 2013;15:1745–58.

  33. 33.

    Lane D J. 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M, editors. Nucleic acid techniques in bacterial systematics. Chichester, United Kingdom: John Wiley and Sons; 1991. pp. 115–175.

  34. 34.

    Turner S, Pryer KM, Miao VPW, Palmer JD. Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA sequence analysis. J Eukaryot Microbiol. 1999;46:327–38.

  35. 35.

    Ovreås L, Forney L, Daae FL, Torsvik V. Distribution of bacterioplankton in meromictic Lake Saelenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA. Appl Environ Microbiol. 1997;63:3367–73.

  36. 36.

    Kolganova TV, Kuznetsov BB, Tourova TP. Designing and testing oligonucleotide primers for amplification and sequencing of archaeal 16S rRNA. Genes. 2002;71:4.

  37. 37.

    Liu H, Probert I, Uitz J, Claustre H, Aris-Brosou S, Frada M, et al. Extreme diversity in noncalcifying haptophytes explains a major pigment paradox in open oceans. Proc Natl Acad Sci USA. 2009;106:12803–08.

  38. 38.

    Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–3.

  39. 39.

    Weiss S, Xu ZZ, Peddada S, Amir A, Bittinger K, Gonzalez A, et al. Normalization and microbial differential abundance strategies depend upon data characteristics. Microbiome 2017;5:27.

  40. 40.

    Wang Q, Garrity GM, Tiedje JM, Cole JR. Naïve bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007;73:5261–7.

  41. 41.

    Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403–10.

  42. 42.

    Guillou L, Bachar D, Audic S, Bass D, Berney C, Bittner L, et al. The protist ribosomal reference database (PR2): a catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy. Nucleic Acids Res. 2013;41:D597–604.

  43. 43.

    Sanchez-Puerta MV, Lippmeier JC, Apt KE, Delwiche CF. Plastid genes in a non-photosynthetic dinoflagellate. Protist. 2007;158:105–17.

  44. 44.

    Lomb NR. Least-squares frequency analysis of unequally spaced data. Astrophys Space Sci. 1976;39:447–62.

  45. 45.

    Scargle JD. Studies in astronomical time series analysis. II-Statistical aspects of spectral analysis of unevenly spaced data. Astrophys J. 1982;263:835–53.

  46. 46.

    Ruf T. The lomb-scargle periodogram in biological rhythm research: analysis of incomplete and unequally spaced time-series. Biol Rhythm Res. 1999;30:178–201.

  47. 47.

    Lê Cao K-A, Rossow D, Robert-Granié C, Besse P. Sparse PLS: Variable selection when integrating omics data. 2008.

  48. 48.

    Nelson JD, Boehme SE, Reimers CE, Sherrell RM, Kerkhof LJ. Temporal patterns of microbial community structure in the mid-atlantic bight: spatio-temporal variability of coastal marine bacteria. FEMS Microbiol Ecol. 2008;65:484–93.

  49. 49.

    Charles F, Lantoine F, Brugel S, Chrétiennot-Dinet M-J, Quiroga I, Rivière B. Seasonal survey of the phytoplankton biomass, composition and production in a littoral NW mediterranean szsite, with special emphasis on the picoplanktonic contribution. Estuar, Coast Shelf Sci. 2005;65:199–212.

  50. 50.

    Marquardt M, Vader A, Stübner EI, Reigstad M, Gabrielsen TM. Strong seasonality of marine microbial eukaryotes in a high-arctic fjord (Isfjorden, in West Spitsbergen, Norway). Appl Environ Microbiol. 2016;82:1868–80.

  51. 51.

    Ward CS, Yung C-M, Davis KM, Blinebry SK, Williams TC, Johnson ZI, et al. Annual community patterns are driven by seasonal switching between closely related marine bacteria. ISME J. 2017;11:1412–22.

  52. 52.

    Monnier A, Liverani S, Bouvet R, Jesson B, Smith JQ, Mosser J, et al. Orchestrated transcription of biological processes in the marine picoeukaryote ostreococcus exposed to light/dark cycles. BMC Genom. 2010;11:192.

  53. 53.

    Eilertsen HC, Sandberg S, Tøllefsen H. Photoperiodic control of diatom spore growth: a theory to explain the onset of phytoplankton blooms. Mar Ecol Progress Ser Oldendorf. 1995;116:303–7.

  54. 54.

    Massana R. Eukaryotic picoplankton in surface o. Annu Rev Microbiol. 2011;65:91–110.

  55. 55.

    Alonso-Sáez L, Díaz-Pérez L, Morán XAG. The hidden seasonality of the rare biosphere in coastal marine bacterioplankton: Seasonality of the rare biosphere. Environ Microbiol. 2015;17:3766–80.

  56. 56.

    Needham DM, Fichot EB, Wang E, Berdjeb L, Cram JA, Fichot CG, et al. Dynamics and interactions of highly resolved marine plankton via automated high-frequency sampling. The ISME J. 2018.

  57. 57.

    Chafee M, Fernàndez-Guerra A, Buttigieg PL, Gerdts G, Eren AM, Teeling H, et al. Recurrent patterns of microdiversity in a temperate coastal marine environment. ISME J. 2018;12:237–52.

  58. 58.

    Alonso-Saez L, Gasol JM. Seasonal variations in the contributions of different bacterial groups to the uptake of low-molecular-weight compounds in northwestern mediterranean coastal waters. Appl Environ Microbiol. 2007;73:3528–35.

  59. 59.

    Paerl RW, Bouget F-Y, Lozano J-C, Vergé V, Schatt P, Allen EE, et al. Use of plankton-derived vitamin B1 precursors, especially thiazole-related precursor, by key marine picoeukaryotic phytoplankton. ISME J. 2017;11:753–65.

  60. 60.

    Carini P, Campbell EO, Morré J, Sañudo-Wilhelmy SA, Cameron Thrash J, Bennett SE, et al. Discovery of a SAR11 growth requirement for thiamin’s pyrimidine precursor and its distribution in the Sargasso Sea. ISME J. 2014;8:1727–38.

  61. 61.

    Paerl RW, Bertrand EM, Allen AE, Palenik B, Azam F. Vitamin B1 ecophysiology of marine picoeukaryotic algae: strain‐specific differences and a new role for bacteria in vitamin cycling. Limnol Oceanogr. 2015;60:215–28.

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We are grateful to the captain and the crew of the RV ‘Nereis II’ for their help in acquiring the samples. We thank the “Service d’Observation”, particularly Eric Maria and Paul Labatut, for their help in obtaining and processing of the samples. MT was supported by a PhD fellowship from the Sorbonne Université and the Région Bretagne. We would like to thank the ABIMS platform in Roscoff for access to bioinformatics resources. This work was supported by the French Agence Nationale de la Recherche through the projects Photo-Phyto (ANR-14-CE02-0018) to FYB, and EUREKA (ANR-14-CE02-0004-01) to PEG.

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  1. CNRS, Laboratoire d’Océanographie Microbienne (LOMIC), Observatoire Océanologique de Banyuls, Sorbonne Université, Banyuls sur Mer, Paris, France

    • Stefan Lambert
    • , Jean-Claude Lozano
    • , Jean-François Ghiglione
    •  & François-Yves Bouget
  2. CNRS, UMR7144, Station Biologique de Roscoff, Sorbonne Université, Roscoff, Paris, France

    • Margot Tragin
    •  & Daniel Vaulot
  3. CNRS, Laboratoire d’Ecogéochimie des Environnements Benthiques (LECOB), Observatoire Océanologique de Banyuls, Sorbonne Université, Banyuls sur Mer, Paris, France

    • Pierre E. Galand


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The authors declare that they have no conflict of interest.

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Correspondence to François-Yves Bouget or Pierre E. Galand.

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