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Response of Marine Bacterioplankton Ph Homeostasis Gene Expression to Elevated CO2

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Response of Marine Bacterioplankton Ph Homeostasis Gene Expression to Elevated CO2 LETTERS PUBLISHED ONLINE: 11 JANUARY 2016 | DOI: 10.1038/NCLIMATE2914 Response of marine bacterioplankton pH homeostasis gene expression to elevated CO2 Carina Bunse1, Daniel Lundin1, Christofer M. G. Karlsson1, Neelam Akram1†, Maria Vila-Costa2†, Joakim Palovaara1†, Lovisa Svensson1, Karin Holmfeldt1, José M. González3, Eva Calvo4, Carles Pelejero4,5, Cèlia Marrasé4, Mark Dopson1, Josep M. Gasol4 and Jarone Pinhassi1* Human-induced ocean acidification impacts marine life. Marine responses of bacterioplankton to changes in seawater pH is bacteria are major drivers of biogeochemical nutrient cycles poor15. This imposes profound limitations in predicting how and energy fluxes1; hence, understanding their performance ocean acidification will affect bacterioplankton involvement in under projected climate change scenarios is crucial for biogeochemical cycling. assessing ecosystem functioning. Whereas genetic and phys- Toinvestigate bacterioplankton (including Bacteria, Cyanobacte- iological responses of phytoplankton to ocean acidification ria and Archaea) responses to projected ocean acidification, we car- are being disentangled2–4, corresponding functional responses ried out a mesocosm experiment with water from the Mediterranean of bacterioplankton to pH reduction from elevated CO2 are Sea. As nutrients are central to determining ocean productivity, essentially unknown. Here we show, from metatranscriptome we chose to maintain mesocosms under two distinct trophic con- analyses of a phytoplankton bloom mesocosm experiment, that ditions: sea water with naturally low-nutrient concentrations ver- marine bacteria responded to lowered pH by enhancing the sus sea water with nutrient-induced phytoplankton blooms. Under expression of genes encoding proton pumps, such as respira- these conditions, a pH reduction of approximately 0.2 units com- tion complexes, proteorhodopsin and membrane transporters. pared with controls was obtained through controlled CO2 bubbling Moreover, taxonomic transcript analysis showed that distinct (Fig.1). Chlorophyll a concentrations (a proxy for phytoplankton bacterial groups expressed dierent pH homeostasis genes in biomass) in the natural seawater mesocosms slowly increased dur- −1 −1 response to elevated CO2. These responses were substantial ing the experiment from 0.6 ± 0.1 µg l to 2.3 ± 0.2 µg l (hereafter, for numerous pH homeostasis genes under low-chlorophyll low-chlorophyll (Low-Chl) mesocosms). In the nutrient-enriched 1 conditions (chlorophyll a<2.5µg l− ); however, the changes in mesocosms, chlorophyll a increased owing to phytoplankton growth gene expression under high-chlorophyll conditions (chlorophyll and peaked at 28.4 ± 4.1 µg l−1 on Day 7, and then decreased 1 a > 20 µg l− ) were low. Given that proton expulsion through until Day 9 (hereafter, high-chlorophyll (High-Chl) mesocosms). pH homeostasis mechanisms is energetically costly, these Following peaks on Day 3–5, bacterial heterotrophic production and findings suggest that bacterioplankton adaptation to ocean abundance in both Low- and High-Chl mesocosms had minima on acidification could have long-term eects on the economy of Day 7, with values increasing again until Day 9 independently of ocean ecosystems. elevated CO2 (two-tailed t-test, p > 0.05; ref. 16). A previous study Anthropogenic emissions of CO2 have caused a significant on 16S ribosomal RNA gene distributions established that elevated decrease in oceanic surface pH, from 8.2 in pre-industrial CO2 did not affect the relative abundance of any bacterial population times to a present value of 8.1 (ref.5). Further reductions in the Low-Chl mesocosms, and only two bacterial populations of 0.3 to 0.4 pH units are projected to occur by the end of responded to acidification in the High-Chl mesocosms17. This pro- this century6, potentially causing pronounced changes in the vided a unique opportunity to directly determine whether or how oceanic carbon cycle4. Recent research on the ecophysiology of natural bacterioplankton adjust their gene expression patterns to individual model algal species and on the structure and function elevated CO2 under contrasting trophic states. of phytoplankton assemblages demonstrates both positive and Sequencing of community messenger RNA obtained at the end of negative effects of reduced pH on ocean primary producers7. the mesocosm experiment (Day 9) yielded between 4 and 11 million Similarly, the magnitude of responses in bacterioplankton activity annotated sequence reads per sample (Supplementary Table 1), and community composition to reductions in seawater pH resulting in identification of 15,798 genes. Grouping of gene varies considerably between experimental studies carried out transcripts into functional metabolic categories showed an overall in different waters and seasons8–13. Given that bacterioplankton dominance of genes related to protein metabolism, membrane account for 12–59% of the surface ocean respiration14, they play transport, and RNA metabolism (Supplementary Fig. 1). Taxonomic a critical role in regulating global biogeochemical cycles of many assignment of transcripts showed that Gammaproteobacteria vital elements1. Yet, mechanistic understanding of physiological dominated in both Low- and High-Chl mesocosms (30–53% of 1Centre for Ecology and Evolution in Microbial Model Systems, EEMiS, Linnaeus University, Barlastgatan 11, 391 82 Kalmar, Sweden. 2Group of Limnology, Department of Continental Ecology, Centre d’Estudis Avançats de Blanes-CSIC, Accés Cala Sant Francesc 14, 17300 Blanes, Catalonia, Spain. 3Department of Microbiology, University of La Laguna, 38200 La Laguna, Spain. 4Departament de Biologia Marina i Oceanografia, Institut de Ciències del Mar—CSIC, Pg. Marítim de la Barceloneta 37-49, 08003 Barcelona, Catalonia, Spain. 5Institució Catalana de Recerca i Estudis Avançats (ICREA), 08010 Barcelona, Catalonia, Spain. †Present addresses: Department of Biosciences, COMSATS Institute of Information Technology, 44000 Islamabad, Pakistan (N.A.); 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.). *e-mail: [email protected] NATURE CLIMATE CHANGE | VOL 6 | MAY 2016 | www.nature.com/natureclimatechange 483 © 2016 Macmillan Publishers Limited. All rights reserved LETTERS NATURE CLIMATE CHANGE DOI: 10.1038/NCLIMATE2914 a 8.4 c ) 40 e −1 d Other Flavobacteria −1 Flavobacteriaceae 30 Other Gammaproteobacteria 8.2 g C l µ Alteromonadaceae Other Alphaproteobacteria 20 pH SAR11 clade 8.0 Rhodobacteraceae 10 8 7.8 Bacterial production ( Bacterial production 0 cpm) 5 6 0123456789 0123456789 10 Time (d) Time (d) × b 40 d 6 4 Low-Chl-acidified ) Low-Chl-control −1 30 High-Chl-acidified ) 2 High-Chl-control 4 −1 cells ml cells g l Counts per million ( Counts 6 µ ( 20 10 a × Chl 2 10 Bacteria ( 0 Low-Chl-control 0123456789 0123456789 igh-Chl-acidifiedHigh-Chl-control Low-Chl-acidified H Time (d) Time (d) Figure 1 | Changes in pH and microbiological parameters during the mesocosm experiments. a, pH levels. b, Chlorophyll a concentrations. c, Bacterial heterotrophic production estimated by leucine incorporation. d, Bacterial abundance. e, Distribution of average relative RNA transcript abundances (normalized to counts per million; CPM) among the four most abundant microbial taxa (averages for duplicate mesocosms). Data in a–d represent averages of duplicate samples ± s.d. Data for panels a–c from ref. 16. annotated reads; Fig.1e). The abundances of Alphaproteobacteria reductase were highly expressed. In several marine bacteria, transcripts were similar in all mesocosms (around 9%), but this reductase is functionally analogous to the canonical proton Bacteroidetes transcripts were ∼4% compared with 11% in the pumping respiratory complex I, essential for energy transduction Low-Chl compared with the High-Chl mesocosms, respectively. and growth of bacteria in low-salinity environments19. In several Ribosomal protein transcripts represented around half of the 50 neutralophilic and acidophilic bacteria, an important strategy most abundant genes (Supplementary Fig. 2). This was in line with to maintain desired intracellular pH in response to acid stress the measured bacterial production, indicating that bacteria in both (resulting from passive proton influx) is to translocate protons Low- and High-Chl mesocosms were metabolically active. across the membrane through respiratory proton pumps20,21. This Statistical analyses identified 303 genes (1.9% of total genes) suggests that the observed pH-induced transcriptional responses in the Low-Chl mesocosms with significant differences in relative in respiration-related genes in the acidified Low-Chl mesocosms transcript abundance (that is, number of transcript reads per would not be primarily for the bacteria to increase their respiration total annotated reads per sample) when comparing acidified with rates (that is, for energetic purposes), but rather as a strategy to cope control mesocosms. Among these, 113 genes had higher abundance with pH stress. whereas the remaining 190 genes had lower abundance in the The most highly expressed gene with significantly different acidified compared with control mesocosms (EdgeR, p<0.01; Fig.2, transcript levels in the acidified Low-Chl mesocosms encoded the Supplementary Fig. 3 and Supplementary Table 2). In contrast, light-driven proton pump proteorhodopsin. The proton motive only 54 genes (0.3% of total
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