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Nutrient recycling facilitates long-term stability of marine microbial phototroph–heterotroph interactions

Nature Microbiology volume 2, Article number: 17100 (2017) Cite this article

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Abstract

Biological interactions underpin the functioning of marine ecosystems, be it via competition, predation, mutualism or symbiosis processes. Microbial phototroph–heterotroph interactions propel the engine that results in the biogeochemical cycling of individual elements, and they are critical for understanding and modelling global ocean processes. Unfortunately, studies thus far have focused on exponentially growing cultures in nutrient-rich media, meaning knowledge of such interactions under in situ conditions is rudimentary at best. Here, we have performed long-term phototroph–heterotroph co-culture experiments under nutrient-amended and natural seawater conditions, and show that it is not the concentration of nutrients but rather their circulation that maintains a stable interaction and a dynamic system. Using the Synechococcus–Roseobacter interaction as a model phototroph–heterotroph case study, we show that although Synechococcus is highly specialized for carrying out photosynthesis and carbon fixation, it relies on the heterotroph to remineralize the inevitably leaked organic matter, making nutrients circulate in a mutualistic system. In this sense we challenge the general belief that marine phototrophs and heterotrophs compete for the same scarce nutrients and niche space, and instead suggest that these organisms more probably benefit from each other because of their different levels of specialization and complementarity within long-term stable-state systems.

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Figure 1: Synechococcus sp. WH7803 grown in axenic (ax) culture and in co-culture with different heterotrophs.
Figure 2: Comparative proteomic analysis of Synechococcus sp. WH7803 proteins detected in the absence (axenic) and presence of R. pomeroyi DSS-3 (co-culture) (n = 3).
Figure 3: Growth curves under nutrient-limiting conditions.
Figure 4: Nutrient analysis.
Figure 5: Schematic representation of the nutrient circulation process taking place in marine phototroph (Synechococcus sp. WH7803)–heterotroph (R. pomeroyi DSS-3) co-cultures in both ASW and seawater conditions.

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References

  1. Jardillier, L., Zubkov, M. V., Pearman, J. & Scanlan, D. J. Significant CO2 fixation by small prymnesiophytes in the subtropical and tropical northeast Atlantic Ocean. ISME J. 4, 1180–1192 (2010).

    Article  CAS  PubMed  Google Scholar 

  2. Scanlan, D. J. et al. Ecological genomics of marine picocyanobacteria. Microbiol. Mol. Biol. Rev. 73, 249–299 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Flombaum, P. et al. Present and future global distributions of the marine cyanobacteria Prochlorococcus and Synechococcus. Proc. Natl Acad. Sci. USA 110, 9824–9829 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Jacquet, S., Prieur, L., Avois-Jacquet, C., Lennon, J.-F. & Vaulot, D. Short-timescale variability of picophytoplankton abundance and cellular parameters in surface waters of the Alboran Sea (western Mediterranean). J. Plankton Res. 24, 635–651 (2002).

    Article  CAS  Google Scholar 

  5. Ribalet, F. et al. Light-driven synchrony of Prochlorococcus growth and mortality in the subtropical Pacific gyre. Proc. Natl Acad. Sci. USA 112, 8008–8012 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. McCarren, J. et al. Microbial community transcriptomes reveal microbes and metabolic pathways associated with dissolved organic matter turnover in the sea. Proc. Natl Acad. Sci. USA 107, 16420–16427 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Sharma, A. K. et al. Distinct dissolved organic matter sources induce rapid transcriptional responses in coexisting populations of Prochlorococcus, Pelagibacter and the OM60 clade. Environ. Microbiol. 16, 2815–2830 (2014).

    Article  CAS  PubMed  Google Scholar 

  8. Biller, S. J. et al. Bacterial vesicles in marine ecosystems. Science 343, 183–186 (2014).

    Article  CAS  PubMed  Google Scholar 

  9. Paver, S. F. et al. Interactions between specific phytoplankton and bacteria affect lake bacterial community succession. Environ. Microbiol. 15, 2489–2504 (2013).

    Article  PubMed  Google Scholar 

  10. Munoz-Marin, M. C. et al. Prochlorococcus can use the Pro1404 transporter to take up glucose at nanomolar concentrations in the Atlantic Ocean. Proc. Natl Acad. Sci. USA 110, 8597–8602 (2013).

    Article  PubMed Central  Google Scholar 

  11. Yelton, A. P. et al. Global genetic capacity for mixotrophy in marine picocyanobacteria. ISME J. 10, 2946–2957 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Christie-Oleza, J. A., Armengaud, J., Guerin, P. & Scanlan, D. J. Functional distinctness in the exoproteomes of marine Synechococcus. Environ. Microbiol. 17, 3781–3794 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Christie-Oleza, J. A., Scanlan, D. J. & Armengaud, J. ‘You produce while I clean up’, a strategy revealed by exoproteomics during Synechococcus–Roseobacter interactions. Proteomics 15, 3454–3462 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Geng, H. & Belas, R. Molecular mechanisms underlying Roseobacter–phytoplankton symbioses. Curr. Opin. Biotechnol. 21, 332–338 (2010).

    Article  CAS  PubMed  Google Scholar 

  15. Hunken, M., Harder, J. & Kirst, G. O. Epiphytic bacteria on the Antarctic ice diatom Amphiprora kufferathii Manguin cleave hydrogen peroxide produced during algal photosynthesis. Plant Biol. 10, 519–526 (2008).

    Article  CAS  PubMed  Google Scholar 

  16. Morris, J. J., Kirkegaard, R., Szul, M. J., Johnson, Z. I. & Zinser, E. R. Facilitation of robust growth of Prochlorococcus colonies and dilute liquid cultures by ‘helper’ heterotrophic bacteria. Appl. Environ. Microbiol. 74, 4530–4534 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Morris, J. J., Johnson, Z. I., Szul, M. J., Keller, M. & Zinser, E. R. Dependence of the cyanobacterium Prochlorococcus on hydrogen peroxide scavenging microbes for growth at the ocean's surface. PLoS ONE 6, e16805 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Sher, D., Thompson, J. W., Kashtan, N., Croal, L. & Chisholm, S. W. Response of Prochlorococcus ecotypes to co-culture with diverse marine bacteria. ISME J. 5, 1125–1132 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Amin, S. A., Parker, M. S. & Armbrust, E. V. Interactions between diatoms and bacteria. Microbiol. Mol. Biol. Rev. 76, 667–684 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Croft, M. T., Lawrence, A. D., Raux-Deery, E., Warren, M. J. & Smith, A. G. Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438, 90–93 (2005).

    Article  CAS  PubMed  Google Scholar 

  21. Sanudo-Wilhelmy, S. A. et al. Multiple B-vitamin depletion in large areas of the coastal ocean. Proc. Natl Acad. Sci. USA 109, 14041–14045 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Grant, M. A., Kazamia, E., Cicuta, P. & Smith, A. G. Direct exchange of vitamin B12 is demonstrated by modelling the growth dynamics of algal-bacterial co-cultures. ISME J. 8, 1418–1427 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Kazamia, E. et al. Mutualistic interactions between vitamin B12-dependent algae and heterotrophic bacteria exhibit regulation. Environ. Microbiol. 14, 1466–1476 (2012).

    Article  CAS  PubMed  Google Scholar 

  24. Durham, B. P. et al. Cryptic carbon and sulfur cycling between surface ocean plankton. Proc. Natl Acad. Sci. USA 112, 453–457 (2015).

    Article  CAS  PubMed  Google Scholar 

  25. Amin, S. A. et al. Interaction and signalling between a cosmopolitan phytoplankton and associated bacteria. Nature 522, 98–101 (2015).

    Article  CAS  PubMed  Google Scholar 

  26. Morris, J. J., Lenski, R. E. & Zinser, E. R. The black queen hypothesis: evolution of dependencies through adaptive gene loss. mBio 3, e00036–12 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  27. Helliwell, K. E. et al. Cyanobacteria and eukaryotic algae use different chemical variants of vitamin B12 . Curr. Biol. 26, 999–1008 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Tai, V., Paulsen, I. T., Phillippy, K., Johnson, D. A. & Palenik, B. Whole-genome microarray analyses of Synechococcus–Vibrio interactions. Environ. Microbiol. 11, 2698–2709 (2009).

    Article  CAS  PubMed  Google Scholar 

  29. Beliaev, A. S. et al. Inference of interactions in cyanobacterial–heterotrophic co-cultures via transcriptome sequencing. ISME J. 8, 2243–2255 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Aharonovich, D. & Sher, D. Transcriptional response of Prochlorococcus to co-culture with a marine Alteromonas: differences between strains and the involvement of putative infochemicals. ISME J. 10, 2892–2906 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Biller, S. J., Coe, A. & Chisholm, S. W. Torn apart and reunited: impact of a heterotroph on the transcriptome of Prochlorococcus. ISME J. 10, 2831–2843 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Parsons, R. J., Breitbart, M., Lomas, M. W. & Carlson, C. A. Ocean time-series reveals recurring seasonal patterns of virioplankton dynamics in the northwestern Sargasso Sea. ISME J. 6, 273–284 (2012).

    Article  CAS  PubMed  Google Scholar 

  33. Mazard, S., Wilson, W. H. & Scanlan, D. J. Dissecting the physiological response to phosphorus stress in marine Synechococcus isolates (Cyanophyceae). J. Phycol. 48, 94–105 (2012).

    Article  CAS  PubMed  Google Scholar 

  34. Mas, A., Jamshidi, S., Lagadeuc, Y., Eveillard, D. & Vandenkoornhuyse, P. Beyond the black queen hypothesis. ISME J. 10, 2085–2091 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  35. Sowell, S. M. et al. Proteomic analysis of stationary phase in the marine bacterium “Candidatus Pelagibacter ubique”. Appl. Environ. Microbiol. 74, 4091–4100 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Grossowicz, M. et al. Prochlorococcus in the lab and in silico: the importance of representing exudation. Limnol. Oceanogr. 62, 818–835 (2017).

    Article  CAS  Google Scholar 

  37. Moran, M. A. et al. Genome sequence of Silicibacter pomeroyi reveals adaptations to the marine environment. Nature 432, 910–913 (2004).

    Article  CAS  PubMed  Google Scholar 

  38. Newton, R. J. et al. Genome characteristics of a generalist marine bacterial lineage. ISME J. 4, 784–798 (2010).

    Article  CAS  PubMed  Google Scholar 

  39. Christie-Oleza, J. A., Fernandez, B., Nogales, B., Bosch, R. & Armengaud, J. Proteomic insights into the lifestyle of an environmentally relevant marine bacterium. ISME J. 6, 124–135 (2012).

    Article  CAS  PubMed  Google Scholar 

  40. Pedler, B. E., Aluwihare, L. I. & Azam, F. Single bacterial strain capable of significant contribution to carbon cycling in the surface ocean. Proc. Natl Acad. Sci. USA 111, 7202–7207 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Arandia-Gorostidi, N., Weber, P. K., Alonso-Saez, L., Moran, X. A. & Mayali, X. Elevated temperature increases carbon and nitrogen fluxes between phytoplankton and heterotrophic bacteria through physical attachment. ISME J. 11, 641–650 (2017).

    Article  CAS  PubMed  Google Scholar 

  42. Lidbury, I. D., Murrell, J. C. & Chen, Y. Trimethylamine and trimethylamine N-oxide are supplementary energy sources for a marine heterotrophic bacterium: implications for marine carbon and nitrogen cycling. ISME J. 9, 760–769 (2015).

    Article  CAS  PubMed  Google Scholar 

  43. Loh, A. N., Bauer, J. E. & Druffel, E. R. Variable ageing and storage of dissolved organic components in the open ocean. Nature 430, 877–881 (2004).

    Article  CAS  PubMed  Google Scholar 

  44. Jiao, N. et al. Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nat. Rev. Microbiol. 8, 593–599 (2010).

    Article  CAS  PubMed  Google Scholar 

  45. Teeling, H. et al. Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science 336, 608–611 (2012).

    Article  CAS  PubMed  Google Scholar 

  46. Weinbauer, M. G. et al. Synechococcus growth in the ocean may depend on the lysis of heterotrophic bacteria. J. Plankton Res. 33, 1465–1476 (2011).

    Article  Google Scholar 

  47. Wilson, W. H., Carr, N. G. & Mann, N. H. The effect of phosphate status on the kinetics of cyanophage infection in the oceanic cyanobacterium Synechococcus sp. WH7803. J. Phycol. 32, 506–516 (1996).

    Article  CAS  Google Scholar 

  48. Lane, D. in Nucleic Acid Techniques in Bacterial Systematics (eds Stackebrandt, E. G. & Goodfellow, M. ) 115–175 (Wiley, 1991).

    Google Scholar 

  49. Hartmann, E. M., Allain, F., Gaillard, J. C., Pible, O. & Armengaud, J. Taking the shortcut for high-throughput shotgun proteomic analysis of bacteria. Methods Mol. Biol. 1197, 275–285 (2014).

    Article  CAS  PubMed  Google Scholar 

  50. de Groot, A. et al. Alliance of proteomics and genomics to unravel the specificities of Sahara bacterium Deinococcus deserti. PLoS Genet. 5, e1000434 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  51. Rivers, A. R., Smith, C. B. & Moran, M. A. An updated genome annotation for the model marine bacterium Ruegeria pomeroyi DSS-3. Stand. Genomic Sci. 9, 11 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  52. Liu, H., Sadygov, R. G. & Yates, J. R. III. A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal. Chem. 76, 4193–4201 (2004).

    Article  CAS  PubMed  Google Scholar 

  53. Masuko, T. et al. Carbohydrate analysis by a phenol-sulfuric acid method in microplate format. Anal. Biochem. 339, 69–72 (2005).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by a NERC Independent Research Fellowship NE/K009044/1, a UK Synthetic Biology Research Centre grant from EPSRC and BBSRC (BB/M017982/1), the EU FP7 project MaCuMBA (grant 311975) and the Commissariat à l'Energie Atomique et aux Energies Alternatives. D.S. was supported by a Central England NERC Training Alliance PhD scholarship via grant NE/L002493/1. The authors also acknowledge technical support from the WPH Proteomic Facility at the University of Warwick.

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Authors and Affiliations

  1. School of Life Sciences, University of Warwick, CV4 7AL, Coventry, UK

    Joseph A. Christie-Oleza, Despoina Sousoni, Matthew Lloyd & David J. Scanlan

  2. CEA, DRF/Joliot/DMTS/SPI/Li2D, Laboratory ‘Technological Innovations for Detection and Diagnostic’, F-30207, Bagnols-sur-Cèze, France

    Jean Armengaud

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Contributions

J.A.C.-O. and D.J.S. conceived the study. J.A.C.-O. designed the experiments. J.A.C.-O., D.S. and M.L. performed the experiments. J.A. carried out the proteomic analyses. J.A.C.-O. analysed the data. J.A.C.-O. and D.J.S. wrote the paper with contributions from J.A.

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Correspondence to Joseph A. Christie-Oleza.

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Christie-Oleza, J., Sousoni, D., Lloyd, M. et al. Nutrient recycling facilitates long-term stability of marine microbial phototroph–heterotroph interactions. Nat Microbiol 2, 17100 (2017). https://doi.org/10.1038/nmicrobiol.2017.100

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