Single-cell measurements and modelling reveal substantial organic carbon acquisition by Prochlorococcus.
Journal
Nature microbiology
ISSN: 2058-5276
Titre abrégé: Nat Microbiol
Pays: England
ID NLM: 101674869
Informations de publication
Date de publication:
12 2022
12 2022
Historique:
received:
14
01
2022
accepted:
13
09
2022
pubmed:
5
11
2022
medline:
3
12
2022
entrez:
4
11
2022
Statut:
ppublish
Résumé
Marine phytoplankton are responsible for about half of the photosynthesis on Earth. Many are mixotrophs, combining photosynthesis with heterotrophic assimilation of organic carbon, but the relative contribution of these two lifestyles is unclear. Here single-cell measurements reveal that Prochlorococcus at the base of the photic zone in the Eastern Mediterranean Sea obtain only ~20% of carbon required for growth by photosynthesis. This is supported by laboratory-calibrated calculations based on photo-physiology parameters and compared with in situ growth rates. Agent-based simulations show that mixotrophic cells could grow tens of metres deeper than obligate photo-autotrophs, deepening the nutricline by ~20 m. Time series from the North Atlantic and North Pacific indicate that, during thermal stratification, on average 8-10% of the Prochlorococcus cells live without enough light to sustain obligate photo-autotrophic populations. Together, these results suggest that mixotrophy underpins the ecological success of a large fraction of the global Prochlorococcus population and its collective genetic diversity.
Identifiants
pubmed: 36329198
doi: 10.1038/s41564-022-01250-5
pii: 10.1038/s41564-022-01250-5
pmc: PMC9712107
doi:
Substances chimiques
Carbon
7440-44-0
Types de publication
Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2068-2077Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2022. The Author(s).
Références
Falkowski, P. G. The role of phytoplankton photosynthesis in global biogeochemical cycles. Photosynth. Res. 39, 235–258 (1994).
Stoecker, D. K., Hansen, P. J., Caron, D. A. & Mitra, A. Mixotrophy in the marine plankton. Annu. Rev. Mar. Sci. 9, 311–335 (2017).
doi: 10.1146/annurev-marine-010816-060617
Hartmann, M. et al. Mixotrophic basis of Atlantic oligotrophic ecosystems. Proc. Natl Acad. Sci. USA 109, 5756–5760 (2012).
pubmed: 22451938
pmcid: 3326507
doi: 10.1073/pnas.1118179109
Zubkov, M. V. & Tarran, G. A. High bacterivory by the smallest phytoplankton in the North Atlantic Ocean. Nature 455, 224–226 (2008). 2008 455:7210.
pubmed: 18690208
doi: 10.1038/nature07236
Ward, B. A. & Follows, M. J. Marine mixotrophy increases trophic transfer efficiency, mean organism size, and vertical carbon flux. Proc. Natl Acad. Sci. USA 113, 2958–2963 (2016).
pubmed: 26831076
pmcid: 4801304
doi: 10.1073/pnas.1517118113
Repeta, D. J. Unifying chemical and biological perspectives of carbon accumulation in the environment. Proc. Natl Acad. Sci. USA https://doi.org/10.1073/pnas.2100935118 (2021).
Zakem, E. J., Cael, B. B. & Levine, N. M. A unified theory for organic matter accumulation. Proc. Natl Acad. Sci. USA 118, e2016896118 (2021).
pubmed: 33536337
pmcid: 8017682
doi: 10.1073/pnas.2016896118
Muñoz-Marín, M. D. 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).
pubmed: 23569224
pmcid: 3666668
doi: 10.1073/pnas.1221775110
Zubkov, M. V., Tarran, G. A. & Fuchs, B. M. Depth related amino acid uptake by Prochlorococcus cyanobacteria in the Southern Atlantic tropical gyre. FEMS Microbiol. Ecol. 50, 153–161 (2004).
pubmed: 19712356
doi: 10.1016/j.femsec.2004.06.009
Muñoz-Marín, M. C. et al. Mixotrophy in marine picocyanobacteria: use of organic compounds by Prochlorococcus and Synechococcus. ISME J. 14, 1065–1073 (2020).
pubmed: 32034281
pmcid: 7174365
doi: 10.1038/s41396-020-0603-9
Biller, S. J., Berube, P. M., Lindell, D. & Chisholm, S. W. Prochlorococcus: the structure and function of collective diversity. Nat. Rev. Microbiol. 13, 13–27 (2015).
pubmed: 25435307
doi: 10.1038/nrmicro3378
Rocap, G., et al. Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424, 1042–1047 (2003).
Coe, A. et al. Survival of Prochlorococcus in extended darkness. Limnol. Oceanogr. 61, 1375–1388 (2016).
doi: 10.1002/lno.10302
Vila-Costa, M. et al. Dimethylsulfoniopropionate uptake by marine phytoplankton. Science 314, 652–654 (2006).
pubmed: 17068265
doi: 10.1126/science.1131043
Becker, J. W., Hogle, S. L., Rosendo, K. & Chisholm, S. W. Co-culture and biogeography of Prochlorococcus and SAR11. ISME J. 13, 1506–1519 (2019).
pubmed: 30742057
pmcid: 6775983
doi: 10.1038/s41396-019-0365-4
Coe, A. et al. Coping with darkness: the adaptive response of marine picocyanobacteria to repeated light energy deprivation. Limnol. Oceanogr. 66, 3300–3312 (2021).
pubmed: 34690365
pmcid: 8518828
doi: 10.1002/lno.11880
Reich, T. et al. A year in the life of the Eastern Mediterranean: Monthly dynamics of phytoplankton and bacterioplankton in an ultra-oligotrophic sea. Deep-Sea Res. Part I 182, 103720 (2022).
doi: 10.1016/j.dsr.2022.103720
Campbell, L. & Vaulot, D. Photosynthetic picoplankton community structure in the subtropical North Pacific Ocean near Hawaii (station ALOHA). Deep Sea Res. Part I 40, 2043–2060 (1993).
doi: 10.1016/0967-0637(93)90044-4
Moore, L. R., Rocap, G. & Chisholm, S. W. Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes. Nature 393, 464–467 (1998).
pubmed: 9624000
doi: 10.1038/30965
Van den Engh, G. J. et al. Dynamics of Prochlorococcus and Synechococcus at station ALOHA revealed through flow cytometry and high-resolution vertical sampling. Front Mar. Sci. 4, 359 (2017).
doi: 10.3389/fmars.2017.00359
Thompson, A. W. et al. Dynamics of Prochlorococcus diversity and photoacclimation during short-term shifts in water column stratification at station ALOHA. Front Mar. Sci. 5, 488 (2018).
doi: 10.3389/fmars.2018.00488
Ahlgren, N. A., Perelman, J. N., Yeh, Y. & Fuhrman, J. A. Multi‐year dynamics of fine‐scale marine cyanobacterial populations are more strongly explained by phage interactions than abiotic, bottom‐up factors. Environ. Microbiol. 21, 2948–2963 (2019).
pubmed: 31106939
doi: 10.1111/1462-2920.14687
Malmstrom, R. R. et al. Temporal dynamics of Prochlorococcus ecotypes in the Atlantic and Pacific oceans. ISME J. 4, 1252–1264 (2010).
pubmed: 20463762
doi: 10.1038/ismej.2010.60
Moore, L. R. & Chisholm, S. W. Photophysiology of the marine cyanobacterium Prochlorococcus: ecotypic differences among cultured isolates. Limnol. Oceanogr. 44, 628–638 (1999).
doi: 10.4319/lo.1999.44.3.0628
Berthelot, H. et al. NanoSIMS single cell analyses reveal the contrasting nitrogen sources for small phytoplankton. ISME J. 13, 651–662 (2019).
pubmed: 30323264
doi: 10.1038/s41396-018-0285-8
Roth-Rosenberg, D. et al. Prochlorococcus cells rely on microbial interactions rather than on chlorotic resting stages to survive long-term nutrient starvation. mBio 11, 1–13 (2020).
doi: 10.1128/mBio.01846-20
Goericke, R. & Welschmeyer, N. A. The marine prochlorophyte Prochlorococcus contributes significantly to phytoplankton biomass and primary production in the Sargasso Sea. Deep Sea Res. Part I 40, 2283–2294 (1993).
doi: 10.1016/0967-0637(93)90104-B
Vaulot, D. The cell cycle of phytoplankton: coupling cell growth to population Growth. In Molecular Ecology of Aquatic Microbes. (ed. Joint, I.) 303–322 (Springer, 1995).
Binder, B. J., Chisholm, S. W., Olson, R. J., Frankel, S. L. & Worden, A. Z. Dynamics of picophytoplankton, ultraphytoplankton and bacteria in the central equatorial Pacific. Deep Sea Res. Part II 43, 907–931 (1996).
doi: 10.1016/0967-0645(96)00023-9
Partensky, F., Blanchot, J., Lantoine, F., Neveux, J. & Marie, D. Vertical structure of picophytoplankton at different trophic sites of the tropical northeastern Atlantic Ocean. Deep Sea Res. Part I 43, 1191–1213 (1996).
doi: 10.1016/0967-0637(96)00056-8
Vaulot, D., Marie, D., Olson, R. J. & Chisholm, S. W. Growth of Prochlorococcus, a photosynthetic prokaryote, in the equatorial Pacific. Ocean. Sci. 268, 1480–1482 (1995).
Liu, H., Nolla, H. & Campbell, L. Prochlorococcus growth rate and contribution to primary production in the equatorial and subtropical North Pacific Ocean. Aquat. Microb. Ecol. 12, 39–47 (1997).
doi: 10.3354/ame012039
Platt, T., Gallegos, C. & Harrison, W. Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J. Mar. Res. 38, 687–701 (1980).
Inomura, K. et al. A mechanistic model of macromolecular allocation, elemental stoichiometry, and growth rate in phytoplankton. Front. Microbiol. 11, 86 (2020).
pubmed: 32256456
pmcid: 7093025
doi: 10.3389/fmicb.2020.00086
Edwards, K. F., Thomas, M. K., Klausmeier, C. A. & Litchman, E. Allometric scaling and taxonomic variation in nutrient utilization traits and maximum growth rate of phytoplankton. Limnol. Oceanogr. 57, 554–566 (2012).
doi: 10.4319/lo.2012.57.2.0554
Lis, H., Shaked, Y., Kranzler, C., Keren, N. & Morel, F. M. M. Iron bioavailability to phytoplankton: an empirical approach. ISME J. 9, 1003–1013 (2014).
pmcid: 4817705
doi: 10.1038/ismej.2014.199
Murray, J., Leinen, M., Feely, R., Toggweiler, R. & Wanninkhof, R. EqPac: a process study in the central equatorial pacific. Oceanography 5, 134–142 (1992).
doi: 10.5670/oceanog.1992.01
Karl, D. M. & Church, M. J. Microbial oceanography and the Hawaii Ocean Time-series programme. Nat. Rev. Microbiol. 12, 699–713 (2014).
Bertilsson, S., Berglund, O., Karl, D. M. & Chisholm, S. W. Elemental composition of marine Prochlorococcus and Synechococcus: implications for the ecological stoichiometry of the sea. Limnol. Oceanogr. 48, 1721–1731 (2003).
doi: 10.4319/lo.2003.48.5.1721
Roth-Rosenberg, D., Aharonovich, D., Omta, A. W., Follows, M. J. & Sher, D. Dynamic macromolecular composition and high exudation rates in Prochlorococcus. Limnol. Oceanogr. 66, 1759–1773 (2021).
doi: 10.1002/lno.11720
Grossowicz, M. et al. Prochlorococcus in the lab and in silico: the importance of representing exudation. Limnol. Oceanogr. 62, 818–835 (2017).
doi: 10.1002/lno.10463
Wu, Z. et al. Modeling photosynthesis and exudation in subtropical oceans. Glob. Biogeochem. Cycles 35, e2021GB006941 (2021).
doi: 10.1029/2021GB006941
Bertlisson, S., Berglund, O., Pullin, M. J. & Chisholm, S. W. Release of dissolved organic matter by Prochlorococcus. Vie Milieu 55, 225–232 (2005).
Yelton, A. P., et al. Global genetic capacity for mixotrophy in marine picocyanobacteria. ISME J. 10, 2946–2957 (2016).
Danovaro, R. Do bacteria compete with phytoplankton for inorganic nutrients? Possible ecological implications. Chem. Ecol. 14, 83–96 (1998).
doi: 10.1080/02757549808035544
Callahan, B. J., et al. DADA2: high-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583 (2016).
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evolution 30, 2725–2729 (2013).
doi: 10.1093/molbev/mst197
Wu, Z. & Forget, G. PlanktonIndividuals.jl: a GPU supported individual-based phytoplankton life cycle model. J. Open Source Softw. 7, 4207 (2022).
doi: 10.21105/joss.04207
Healey, F. P. Interacting effects of light and nutrient limitation on the growth rate of Synechococcus linearis (Cyanophyceae). J. Phycol. 21, 134–146 (1985).
doi: 10.1111/j.0022-3646.1985.00134.x