Abstract
Submerged angiosperms sustain some of the most productive and diverse ecosystems worldwide. However, their carbon acquisition and assimilation mechanisms remain poorly explored, missing an important step in the evolution of photosynthesis during the colonization of aquatic environments by angiosperms. Here we reveal a convergent kinetic adaptation of Rubisco in phylogenetically distant seagrass species that share catalytic efficiencies and CO2 and O2 affinities up to three times lower than those observed in phylogenetically closer angiosperms from terrestrial, freshwater and brackish-water habitats. This Rubisco kinetic convergence was found to correlate with the effectiveness of seagrass CO2-concentrating mechanisms (CCMs), which probably evolved in response to the constant CO2 limitation in marine environments. The observed Rubisco kinetic adaptation in seagrasses more closely resembles that seen in eukaryotic algae operating CCMs rather than that reported in terrestrial C4 plants. Our results thus demonstrate a general pattern of co-evolution between Rubisco function and biophysical CCM effectiveness that traverses distantly related aquatic lineages.
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Data availability
All processed data are contained in the manuscript or in the supplementary data files. The 61 rbcL sequences used in this study were extracted from GenBank at https://www.ncbi.nlm.nih.gov/nuccore (see the accession numbers in Supplementary Fig. 1). The reference rbcL sequence of Spinacia oleracea is under accession number NC 002202.1 in GenBank. The kinetic data used for Fig. 2 were extracted from Iñiguez et al.21 (the data are freely available at https://onlinelibrary.wiley.com/doi/10.1111/tpj.14643) and Goudet et al.23 (the data are freely available at https://nph.onlinelibrary.wiley.com/doi/full/10.1111/nph.16577). The spinach three-dimensional Rubisco structure used in Extended Data Fig. 3 is available at PDB under accession number 1UPM (https://www.rcsb.org/structure/1UPM). Source data are provided with this paper.
Change history
29 June 2022
A Correction to this paper has been published: https://doi.org/10.1038/s41477-022-01203-0
References
Duarte, B. et al. Climate Change impacts on seagrass meadows and macroalgal forests: an integrative perspective on acclimation and adaptation potential. Front. Mar. Sci. 5, 190 (2018).
Costanza, R. et al. Changes in the global value of ecosystem services. Glob. Environ. Change 26, 152–158 (2014).
Zeebe, R. E. On the molecular diffusion coefficients of dissolved CO2, HCO3−, and CO32− and their dependence on isotopic mass. Geochim. Cosmochim. Acta 75, 2483–2498 (2011).
Mass, T., Genin, A., Shavit, U., Grinstein, M. & Tchernov, D. Flow enhances photosynthesis in marine benthic autotrophs by increasing the efflux of oxygen from the organism to the water. Proc. Natl Acad. Sci. USA 107, 2527–2531 (2010).
Skirrow, G. in Chemical Oceanography Vol. 2 (eds Riley, J. P. & Skirrow, G.) 192 (Academic Press, 1975).
Stumm, W. & Morgan, J. J. Aquatic Chemistry: Chemical Equilibria in Natural Waters (John Wiley & Sons, 2012).
Maberly, S. C. & Gontero, B. Ecological imperatives for aquatic CO2-concentrating mechanisms. J. Exp. Bot. 68, 3797–3814 (2017).
Maberly, S. C. Diel, episodic and seasonal changes in pH and concentrations of inorganic carbon in a productive lake. Freshw. Biol. 35, 579–598 (1996).
Meybeck, M. in Treatise on Geochemistry (eds Holland, H. D. & Turekian, K. K.) Vol. 5, 207–223 (Elsevier Science, 2003).
Giordano, M., Beardall, J. & Raven, J. A. CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu. Rev. Plant Biol. 56, 99–131 (2005).
Beer, S., Shomer-Ilan, A. & Waisel, Y. Carbon metabolism in seagrasses. J. Exp. Bot. 31, 1027–1033 (1980).
Raven, J. A., Cockell, C. S. & De La Rocha, C. L. The evolution of inorganic carbon concentrating mechanisms in photosynthesis. Phil. Trans. R. Soc. B 363, 2641–2650 (2008).
Yin, L., Li, W., Madsen, T. V., Maberly, S. C. & Bowes, G. Photosynthetic inorganic carbon acquisition in 30 freshwater macrophytes. Aquat. Bot. 140, 48–54 (2017).
Larkum, A. W. D., Davey, P. A., Kuo, J., Ralph, P. J. & Raven, J. A. Carbon-concentrating mechanisms in seagrasses. J. Exp. Bot. 68, 3773–3784 (2017).
Raven, J. A., Beardall, J. & Sánchez-Baracaldo, P. The possible evolution and future of CO2-concentrating mechanisms. J. Exp. Bot. 68, 3701–3716 (2017).
Meyer, M. & Griffiths, H. Origins and diversity of eukaryotic CO2-concentrating mechanisms: lessons for the future. J. Exp. Bot. 64, 769–786 (2013).
Badger, M. R. et al. The diversity and coevolution of Rubisco, plastids, pyrenoids, and chloroplast-based CO2-concentrating mechanisms in algae. Can. J. Bot. 76, 1052–1071 (1998).
Savir, Y., Noor, E., Milo, R. & Tlusty, T. Cross-species analysis traces adaptation of Rubisco toward optimality in a low-dimensional landscape. Proc. Natl Acad. Sci. USA 107, 3475–3480 (2010).
Tcherkez, G. G. B., Farquhar, G. D. & Andrews, T. J. Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized. Proc. Natl Acad. Sci. USA 103, 7246–7251 (2006).
Flamholz, A. I. et al. Revisiting trade-offs between Rubisco kinetic parameters. Biochemistry 58, 3365–3376 (2019).
Iñiguez, C. et al. Evolutionary trends in RuBisCO kinetics and their co-evolution with CO2 concentrating mechanisms. Plant J. 101, 897–918 (2020).
Genkov, T. & Spreitzer, R. J. Highly conserved small subunit residues influence Rubisco large subunit catalysis. J. Biol. Chem. 284, 30105–30112 (2009).
Goudet, M. M. M. et al. Rubisco and carbon-concentrating mechanism co-evolution across chlorophyte and streptophyte green algae. N. Phytol. 227, 810–823 (2020).
Heureux, A. M. C. et al. The role of Rubisco kinetics and pyrenoid morphology in shaping the CCM of haptophyte microalgae. J. Exp. Bot. 68, 3959–3969 (2017).
Young, J. N. et al. Large variation in the Rubisco kinetics of diatoms reveals diversity among their carbon-concentrating mechanisms. J. Exp. Bot. 67, 3445–3456 (2016).
Lucas, W. J. Photosynthetic assimilation of exogenous HCO3− by aquatic plants. Annu. Rev. Plant Physiol. 34, 71–104 (1983).
Walker, N. A., Smith, F. A. & Cathers, I. R. Bicarbonate assimilation by fresh-water charophytes and higher plants: I. Membrane transport of bicarbonate ions is not proven. J. Membr. Biol. 57, 51–58 (1980).
Rubio, L. et al. Direct uptake of HCO3− in the marine angiosperm Posidonia oceanica (L.) Delile driven by a plasma membrane H+ economy. Plant Cell Environ. 40, 2820–2830 (2017).
Iñiguez, C., Galmés, J. & Gordillo, F. J. L. Rubisco carboxylation kinetics and inorganic carbon utilization in polar versus cold-temperate seaweeds. J. Exp. Bot. 70, 1283–1297 (2019).
Capó-Bauçà, S., Font-Carrascosa, M., Ribas-Carbó, M., Pavlovič, A. & Galmés, J. Biochemical and mesophyll diffusional limits to photosynthesis are determined by prey and root nutrient uptake in the carnivorous pitcher plant Nepenthes × ventrata. Ann. Bot. 126, 25–37 (2020).
Evans, J. R. Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78, 9–19 (1989).
Raven, J. A. & Beardall, J. The ins and outs of CO2. J. Exp. Bot. 67, 1–13 (2016).
Mohr, W. et al. Terrestrial-type nitrogen-fixing symbiosis between seagrass and a marine bacterium. Nature 600, 105–109 (2021).
Larkum, A. W. D., Orth, R. J. & Duarte, C. M. Seagrass: Biology, Ecology and Conservation (Springer Netherlands, 2006); https://doi.org/10.1007/978-1-4020-2983-7
Les, D. H., Cleland, M. A. & Waycott, M. Phylogenetic studies in Alismatidae, II: evolution of marine angiosperms (seagrasses) and hydrophily. Syst. Bot. 22, 443–463 (1997).
Ishikawa, C., Hatanaka, T., Misoo, S., Miyake, C. & Fukayama, H. Functional incorporation of sorghum small subunit increases the catalytic turnover rate of Rubisco in transgenic rice. Plant Physiol. 156, 1603–1611 (2011).
Lin, M. T., Stone, W. D., Chaudhari, V. & Hanson, M. R. Small subunits can determine enzyme kinetics of tobacco Rubisco expressed in Escherichia coli. Nat. Plants 6, 1289–1299 (2020).
Raven, J. A., Ball, L. A., Beardall, J., Giordano, M. & Maberly, S. C. Algae lacking carbon-concentrating mechanisms. Can. J. Bot. 83, 879–890 (2005).
Young, J. N. & Hopkinson, B. M. The potential for co-evolution of CO2-concentrating mechanisms and Rubisco in diatoms. J. Exp. Bot. 68, 3751–3762 (2017).
Griffiths, H., Meyer, M. T. & Rickaby, R. E. M. Overcoming adversity through diversity: aquatic carbon concentrating mechanisms. J. Exp. Bot. 68, 3689–3695 (2017).
Farquhar, G., Caemmerer, S., Von & Berry, J. A. A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 90, 78–90 (1980).
Winkel, A. & Borum, J. Use of sediment CO2 by submersed rooted plants. Annals of Botany. 103, 1015–1023 (2009).
Galmés, J. et al. Environmentally driven evolution of Rubisco and improved photosynthesis and growth within the C3 genus Limonium (Plumbaginaceae). N. Phytol. 203, 989–999 (2014).
Sharwood, R. E., Ghannoum, O., Kapralov, M. V., Gunn, L. H. & Whitney, S. M. Temperature responses of Rubisco from Paniceae grasses provide opportunities for improving C 3 photosynthesis. Nat. Plants 2, 16186 (2016).
Wissler, L. et al. Back to the sea twice: identifying candidate plant genes for molecular evolution to marine life. BMC Evol. Biol. 11, 8 (2011).
Larkum, A. W. D., Kendrick, G. A. & Ralph, P. J. (eds) Seagrasses of Australia (Springer Cham, 2018).
Berner, R. A. & Kothavala, Z. Geocarb III: a revised model of atmospheric CO2 over Phanerozoic time. Am. J. Sci. 301, 182–204 (2001).
Sage, R. F., Monson, R. K., Ehleringer, J. R., Adachi, S. & Pearcy, R. W. Some like it hot: the physiological ecology of C4 plant evolution. Oecologia 187, 941–966 (2018).
Chen, L. Y., Chen, J. M., Gituru, R. W. & Wang, Q. F. Generic phylogeny, historical biogeography and character evolution of the cosmopolitan aquatic plant family Hydrocharitaceae. BMC Evol. Biol. 12, 30 (2012).
Janssen, T. & Bremer, K. The age of major monocot groups inferred from 800+ rbcL sequences. Bot. J. Linn. Soc. 146, 385–398 (2004).
Lindqvist, C. et al. Molecular phylogenetics of an aquatic plant lineage, Potamogetonaceae. Cladistics 22, 568–588 (2006).
Yao, G. et al. Phylogenetic relationships, character evolution and biogeographic diversification of Pogostemon s.l. (Lamiaceae). Mol. Phylogenet. Evol. 98, 184–200 (2016).
Wang, H. & Dilcher, D. L. A new species of Donlesia (Ceratophyllaceae) from the Early Cretaceous of Kansas, USA. Rev. Palaeobot. Palynol. 252, 20–28 (2018).
Bouvier, J. W. et al. Rubisco adaptation is more limited by phylogenetic constraint than by catalytic trade-off. Mol. Biol. Evol. 38, 2880–2896 (2021).
Kim, M. et al. Low oxygen affects photophysiology and the level of expression of two-carbon metabolism genes in the seagrass Zostera muelleri. Photosynth. Res. 136, 147–160 (2018).
Roberts, D. G. & Moriarty, D. J. W. Lacunal gas discharge as a measure of productivity in the seagrasses Zostera capricorni, Cymodocea serrulata and Syringodium isoetifolium. Aquat. Bot. 28, 143–160 (1987).
Bowes, G., Rao, S. K., Estavillo, G. M. & Reiskind, J. B. C4 mechanisms in aquatic angiosperms: comparisons with terrestrial C4 systems. Funct. Plant Biol. 29, 379–392 (2002).
Invers, O., Zimmerman, R. C., Alberte, R. S., Pérez, M. & Romero, J. Inorganic carbon sources for seagrass photosynthesis: an experimental evaluation of bicarbonate use in species inhabiting temperate waters. J. Exp. Mar. Biol. Ecol. 265, 203–217 (2001).
Lewis, E. & Wallace, D. Program Developed for CO2 System Calculations (Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, 1998).
Price, G. & Badger, M. Inhibition by proton buffers of photosynthetic utilization of bicarbonate in Chara corallina. Aust. J. Plant Physiol. 12, 257–267 (1985).
Beer, S., Bjork, M., Hellblom, F. & Axelsson, L. Inorganic carbon utilization in marine angiosperms (seagrasses). Funct. Plant Biol. 29, 349–354 (2002).
Galmés, J., Medrano, H. & Flexas, J. Photosynthetic limitations in response to water stress and recovery in Mediterranean plants with different growth forms. N. Phytol. 175, 81–93 (2007).
Flexas, J. et al. Analysis of leakage in IRGA’s leaf chambers of open gas exchange systems: quantification and its effects in photosynthesis parameterization. J. Exp. Bot. 58, 1533–1543 (2007).
Iñiguez, C. et al. Increased temperature, rather than elevated CO2, modulates the carbon assimilation of the Arctic kelps Saccharina latissima and Laminaria solidungula. Mar. Biol. 163, 248 (2016).
Galmés, J. et al. Expanding knowledge of the Rubisco kinetics variability in plant species: environmental and evolutionary trends. Plant Cell Environ. 37, 1989–2001 (2014).
Ruuska, S. et al. The interplay between limiting processes in C3 photosynthesis studied by rapid-response gas exchange using transgenic tobacco impaired in photosynthesis. Aust. J. Plant Physiol. 25, 859–870 (1998).
Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal. Biochem. 72, 248–254 (1976).
Sharwood, R. E., Von Caemmerer, S., Maliga, P. & Whitney, S. M. The catalytic properties of hybrid Rubisco comprising tobacco small and sunflower large subunits mirror the kinetically equivalent source Rubiscos and can support tobacco growth. Plant Physiol. 146, 83–96 (2008).
Kane, H. et al. An improved method for measuring the CO2/O2 specificity of ribulosebisphosphate carboxylase–oxygenase. Aust. J. Plant Physiol. 21, 449–461 (1994).
Galmés, J., Hermida-Carrera, C., Laanisto, L. & Niinemets, Ü. A compendium of temperature responses of Rubisco kinetic traits: variability among and within photosynthetic groups and impacts on photosynthesis modeling. J. Exp. Bot. 67, 5067–5091 (2016).
Archontoulis, S. V., Yin, X., Vos, J., Danalatos, N. G. & Struik, P. C. Leaf photosynthesis and respiration of three bioenergy crops in relation to temperature and leaf nitrogen: how conserved are biochemical model parameters among crop species? J. Exp. Bot. 63, 895–911 (2012).
Hedges, S. B., Marin, J., Suleski, M., Paymer, M. & Kumar, S. Tree of life reveals clock-like speciation and diversification. Mol. Biol. Evol. 32, 835–845 (2015).
Kumar, S., Stecher, G., Suleski, M. & Hedges, S. B. TimeTree: a resource for timelines, timetrees, and divergence times. Mol. Biol. Evol. 34, 1812–1819 (2017).
Tamura, K. Estimation of the number of nucleotide substitutions when there are strong transition–transversion and G+C-content biases. Mol. Biol. Evol. 9, 678–687 (1992).
Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547–1549 (2018).
Yang, Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591 (2007).
Zhang, J., Nielsen, R. & Yang, Z. Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol. Biol. Evol. 22, 2472–2479 (2005).
Acknowledgements
This work was financially supported by the Spanish Ministry of Sciences, Innovation and Universities, the Spanish State Research Agency and the European Regional Development Funds (project no. PGC2018-094621-B-I00) awarded to J.G. S.C.-B. was supported by an FPU Grant from the Spanish Ministry of Education. C.I. was supported by a postdoctoral grant from the government of the Balearic Islands. We thank T. Garcia for technical help and organization of the radioisotope installation at the Serveis Científico-Tècnics (UIB); M. Ribas-Carbó, C. Douthe and B. Martorell for their technical help on the IRMS; and Jardí Botànic de Sóller, M. Mus, A. Martínez, J. Rita, X. Gago, F. Tomas, J. Máñez-Crespo, Á. Mateo-Ramírez, M. Fullana and M. Del Río Buzón for their help in the identification and sampling of the species. We thank X. Niell for comments that helped improve this manuscript.
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C.I. and J.G. conceived and designed the study. S.C.-B. performed the experiments, analysed the data and produced the figures with help from all authors. P.A.-N. collaborated in the processing of the samples. S.C.-B. wrote most of the manuscript with help from all authors.
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Extended data
Extended Data Fig. 1 Net photosynthetic rates under different pH.
a, freshwater species (P = 8.3 ×10−7 in C. demersum and P = 0.0002 in V. gigantea); b, brackish water species (P = 3.3 ×10−8 in S. pectinata and P = 8.6 ×10−11 in R. cirrhosa); c, seawater species (P = 8.2 ×10−5 in P. oceanica, P = 0.1601 in C. nodosa, P = 0.3993 in Z. noltii and P = 5.7 ×10−6 in Z. marina). Points are means ± s.e. Different letters show significant differences among net photosynthetic rates. P values were obtained from the F-statistic of one-way ANOVA or from the chi-squared value of Kruskal–Wallis test in the case of non-parametric data. Duncan’s test and Kruskal–Wallis test followed by Bonferroni correction for non-parametric data were used to detect differences among means.
Extended Data Fig. 2 Principal Component Analysis of the CO2 concentrating mechanism proxies analysed.
Variables included are: isotopic discrimination of 13C of leaf biomass (δ13C), pH compensation point determined by pH-drift assay (pH*), in vivo photosynthetic semi-saturation constant for CO2 (Km CO2) and for dissolved inorganic carbon (Km DIC), percentage of the net photosynthetic rate inhibition after addition of acetazolamide (AZ), ethoxyzolamide (EZ), TRIS-buffer (TRIS) and 4,40-diisothiocyanatostilbene-2,20-disulfonate (DIDS), and the percentage of the net photosynthetic rate variation at pH 9-9.5 (An rate at high pH) and at pH 7-7.5 (An rate at low pH) relative to water environmental pH (pH ~8).
Extended Data Fig. 3 rbcL and amino acid Rubisco large subunit analyses.
a, Maximum likelihood tree inferred from the rbcL of the species selected in this study. Bootstrap values (from 1000 replicates) are indicated at the nodes. Colour names indicate the environment of the species: blue are seagrasses species, red are brackish- water species, green are freshwater species and orange terrestrial species. b, Alignment of the rbcL amino acid sequences from the species belonging to the two main branches identified in the previous maximum likelihood tree containing the analysed seagrasses. In blue, amino acid changes among Stuckenia pectinata, and Zostera species; in red, amino acid changes between Ruppia cirrhosa and Posidonia oceanica; in green, amino acid changes between Ruppia cirrhosa and Cymodocea nodosa. Amino acids in boxes denote differences between Z. noltii and Z. marina and amino acid changes shared by C. nodosa and P. oceanica. c, localisation of variable amino acid sites between R. cirrhosa and P. oceanica. d, localisation of variable amino acid sites between R. cirrhosa and C. nodosa. e, localisation of variable amino acid sites between Stuckenia pectinata and Zostera species. f, localisation of variable amino acid sites between Z. noltii and Z. marina. Two L-subunits forming a functional dimer are highlighted in green and cyan in all Rubisco structures showed. Rubisco L-subunit residues are presented on the structure of spinach Rubisco (1UPM) using UCSF Chimera V1.12. Note: The large phylogenetic distance among the species made difficult to relate the particularities of Rubisco catalytic properties of seagrasses to specific amino acid changes. However, the two congeneric Zostera species included in the study only differed at positions 249 and 353 of the Rubisco large subunit sequence (Extended Data Fig. 3f), which coincide with a significantly lower Sc/o in Z. noltii compared with Z. marina (Table 1).
Extended Data Fig. 4 Modelled Rubisco gross assimilation rate (ARub) for the analysed aquatic species.
Solid line, seagrasses; dotted line, brackish water species; dashed line, freshwater species. The photosynthesis model of Farquhar et al. 41 was used to model ARub at the different concentrations of chloroplastic CO2 (Cc). This modelling exercise was done assuming CO2 assimilation rates under saturating light conditions and Rubisco content standardized to 1 g m−2.
Extended Data Fig. 5 Modelled leaf net photosynthetic rate as a function of chloroplastic CO2 (Cc) using equations of the photosynthetic C3 model of Farquhar et al. 7 and the Rubisco kinetic data for each species.
a, P. oceanica; b, Z. noltii; c, Z. marina; d, C. nodosa; e, S. pectinata; f, R. cirrhosa; g, C. demersum; h, V. gigantea; i, T. maritima; j, A. lanceolatum. In blue is respresented the Rubisco-limited rate of CO2 assimilation (Ac) and in green, the electron-transport limited rate of CO2 assimilation (Aj). The equivalent extracellular CO2 concentration (Ca) is shown in the upper x axis.The Cc and Ca where Aj = Ac are indicated by black and red arrows, respectively.
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Capó-Bauçà, S., Iñiguez, C., Aguiló-Nicolau, P. et al. Correlative adaptation between Rubisco and CO2-concentrating mechanisms in seagrasses. Nat. Plants 8, 706–716 (2022). https://doi.org/10.1038/s41477-022-01171-5
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DOI: https://doi.org/10.1038/s41477-022-01171-5
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