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Response of marine bacterioplankton pH homeostasis gene expression to elevated CO2

Nature Climate Change volume 6, pages 483–487 (2016)Cite this article

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Abstract

Human-induced ocean acidification impacts marine life. Marine bacteria are major drivers of biogeochemical nutrient cycles and energy fluxes1; hence, understanding their performance under projected climate change scenarios is crucial for assessing ecosystem functioning. Whereas genetic and physiological responses of phytoplankton to ocean acidification are being disentangled2,3,4, corresponding functional responses of bacterioplankton to pH reduction from elevated CO2 are essentially unknown. Here we show, from metatranscriptome analyses of a phytoplankton bloom mesocosm experiment, that marine bacteria responded to lowered pH by enhancing the expression of genes encoding proton pumps, such as respiration complexes, proteorhodopsin and membrane transporters. Moreover, taxonomic transcript analysis showed that distinct bacterial groups expressed different pH homeostasis genes in response to elevated CO2. These responses were substantial for numerous pH homeostasis genes under low-chlorophyll conditions (chlorophyll a <2.5 μg l−1); however, the changes in gene expression under high-chlorophyll conditions (chlorophyll a >20 μg l−1) were low. Given that proton expulsion through pH homeostasis mechanisms is energetically costly, these findings suggest that bacterioplankton adaptation to ocean acidification could have long-term effects on the economy of ocean ecosystems.

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Figure 1: Changes in pH and microbiological parameters during the mesocosm experiments.
Figure 2: Bacterioplankton gene expression response under elevated CO2.
Figure 3: Model of bacterial strategies for pH homeostasis on acid stress.

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Acknowledgements

The skilful technical assistance of S. Arnautovic, V. Balague, C. Cardelús, L. Cros, E. Vázquez-Domínguez, J. Movilla and À. López-Sanz made this experiment possible. We thank Anselm and the CEAB boat crew for assistance with sampling and M. A. Moran for insightful comments on our work. This research was financially supported by grants from the Göran Gustafsson Foundation for Research in Natural Sciences and Medicine, the Swedish Research Council VR, the Swedish Research Council FORMAS strong research programme EcoChange, and the BONUS BLUEPRINT project, which has received funding from BONUS, the joint Baltic Sea research and development programme (Art 185), funded jointly from the European Union’s Seventh Programme for research, technological development and demonstration and from the Swedish Research Council FORMAS to J.Pinhassi. The research was also financially supported by the Spanish Ministry of Science and Innovation project DOREMI (CTM2012-34294) to C.M. and J.M.Gasol, and by project CTM2013-48292-C3-3-R to J.M.Gasol. 

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Author notes

  1. Neelam Akram, Maria Vila-Costa & Joakim Palovaara

    Present address: Present addresses: Department of Environmental Chemistry, IDAEA-CSIC, Jordi Girona 18-24, 08034 Barcelona, Catalunya, Spain (M.V.-C.); Department of Agrotechnology and Food Sciences, Wageningen University, 6703HA Wageningen, The Netherlands (J.P.); Department of Biosciences, COMSATS Institute of Information Technology, 44000 Islamabad, Pakistan (N.A.).,

Authors and Affiliations

  1. Centre for Ecology and Evolution in Microbial Model Systems, EEMiS, Linnaeus University, Barlastgatan 11, 391 82 Kalmar, Sweden

    Carina Bunse, Daniel Lundin, Christofer M. G. Karlsson, Neelam Akram, Joakim Palovaara, Lovisa Svensson, Karin Holmfeldt, Mark Dopson & Jarone Pinhassi

  2. Department of Continental Ecology, Group of Limnology, Centre d’Estudis Avançats de Blanes-CSIC, Accés Cala Sant Francesc 14, 17300 Blanes, Catalonia, Spain

    Maria Vila-Costa

  3. Department of Microbiology, University of La Laguna, 38200 La Laguna, Spain

    José M. González

  4. Departament de Biologia Marina i Oceanografia, Institut de Ciències del Mar—CSIC, Pg. Marítim de la Barceloneta 37-49, 08003 Barcelona, Catalonia, Spain

    Eva Calvo, Carles Pelejero, Cèlia Marrasé & Josep M. Gasol

  5. Institució Catalana de Recerca i Estudis Avançats (ICREA), 08010 Barcelona, Catalonia, Spain

    Carles Pelejero

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Contributions

M.D., C.P., J.M.Gasol and J.Pinhassi conceived the study. C.P., C.M., J.M.Gasol and J.Pinhassi designed research. N.A., M.V.-C., J.M.González, E.C., C.P., C.M., J.M.Gasol and J.Pinhassi carried out the mesocosm experiment and collected samples for microbial and chemical analyses. E.C. and C.M. measured and adjusted pH. N.A., M.V.-C. and J.Palovaara carried out RNA extraction. C.B., D.L., C.M.G.K., L.S., K.H., J.M.González, M.D. and J.Pinhassi analysed data. C.B., D.L. and J.Pinhassi wrote the paper with help from C.M.G.K., L.S. and M.D. All authors discussed the results and commented on the manuscript.

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Correspondence to Jarone Pinhassi.

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Bunse, C., Lundin, D., Karlsson, C. et al. Response of marine bacterioplankton pH homeostasis gene expression to elevated CO2. Nature Clim Change 6, 483–487 (2016). https://doi.org/10.1038/nclimate2914

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