No adaptation to warming after selection for 800 generations in the coccolithophore Emiliania huxleyi BOF 92

Ocean warming is suggested to exert profound effects on phytoplankton physiology and growth. Here, we investigated how the coccolithophore Emiliania huxleyi (BOF 92, a non-calcifying strain) responded to changes in temperature in short- and long-term thermal treatments. The specific growth rate after 10 days of acclimation increased gradually with increasing temperatures (14, 17, 21, 24, 28°C) and peaked at ~23°C, followed by a significant decrease to 28°C. Chlorophyll a content, cell size, photosynthetic rate, and respiratory rate increased significantly from 14°C to 24°C, but the cellular particulate organic carbon (POC) and nitrogen (PON) showed the lowest values at the optimal temperature. In contrast, during long-term thermal treatments at 17°C and 21°C for 656 days (~790 generations for 17°C treatment; ~830 generations for 21°C treatment), the warming significantly stimulated the growth in the first 34 days and the last 162 days, but there was no significant difference in specific growth rate from Day 35 to Day 493. Chlorophyll a content, cell size, cellular POC/PON, and the ratio of POC to PON, showed no significant difference between the warming and control for most of the duration of the long-term exposure. The warming-selected population did not acquire persistent traits in terms of growth and cell quotas of POC and PON, which resumed to the levels in the control temperature treatment after about 9 generations in the shift test. In summary, our results indicate that warming by 4°C (17°C and 21°C) enhanced the growth, but did not result in adaptative changes in E. huxleyi (BOF 92) over a growth period of about 800 generations, reflecting that mild or non-stressful warming treatment to E. huxleyi isolated from cold seas does not alter its phenotypic plasticity.

[1]  Ruiping Huang,et al.  Reallocation of elemental content and macromolecules in the coccolithophore Emiliania huxleyi to acclimate to climate change , 2023, Biogeosciences.

[2]  Yan Zhang,et al.  Plastic responses lead to increased neurotoxin production in the diatom Pseudo-nitzschia under ocean warming and acidification , 2023, The ISME Journal.

[3]  K. Gao,et al.  Reduced salinity exacerbates the viral infection on the coccolithophorid Emiliania huxleyi at elevated pCO2 , 2022, Frontiers in Marine Science.

[4]  K. Gao,et al.  Increased genetic diversity loss and genetic differentiation in a model marine diatom adapted to ocean warming compared to high CO2 , 2022, The ISME Journal.

[5]  Lin Lin,et al.  Metabolic Adaptation of a Globally Important Diatom following 700 Generations of Selection under a Warmer Temperature. , 2022, Environmental science & technology.

[6]  D. Roberts,et al.  The Ocean and Cryosphere in a Changing Climate , 2022 .

[7]  K. Gao.  Approaches and involved principles to control pH/pCO2 stability in algal cultures , 2021, Journal of Applied Phycology.

[8]  J. Xia,et al.  Adaptation of a marine diatom to ocean acidification and warming reveals constraints and trade-offs. , 2021, The Science of the total environment.

[9]  K. Gao,et al.  Light availability modulates the effects of warming in a marine N2 fixer , 2019, Biogeosciences.

[10]  Dedmer B. Van de Waal,et al.  Meta‐analysis reveals enhanced growth of marine harmful algae from temperate regions with warming and elevated CO2 levels , 2019, Global change biology.

[11]  Petra Hendriks,et al.  Analyzing the Time Course of Pupillometric Data , 2019, Trends in hearing.

[12]  S. Agustí,et al.  Fast adaptation of tropical diatoms to increased warming with trade-offs , 2018, Scientific Reports.

[13]  K. Gao,et al.  Adaptive evolution in the coccolithophore Gephyrocapsa oceanica following 1,000 generations of selection under elevated CO2 , 2018, Global change biology.

[14]  A. Buckling,et al.  Environmental fluctuations accelerate molecular evolution of thermal tolerance in a marine diatom , 2017, bioRxiv.

[15]  S. Wood.  Generalized Additive Models: An Introduction with R, Second Edition , 2017 .

[16]  A. Buckling,et al.  Adaptation of phytoplankton to a decade of experimental warming linked to increased photosynthesis , 2017, Nature Ecology &Evolution.

[17]  Elena Litchman,et al.  Phytoplankton growth and the interaction of light and temperature: A synthesis at the species and community level , 2016 .

[18]  Mridul K. Thomas,et al.  Swift thermal reaction norm evolution in a key marine phytoplankton species , 2016, Evolutionary applications.

[19]  A. Buckling,et al.  Rapid evolution of metabolic traits explains thermal adaptation in phytoplankton , 2015, Ecology letters.

[20]  R. Geider,et al.  Acclimation of E miliania huxleyi (1516) to nutrient limitation involves precise modification of the proteome to scavenge alternative sources of N and P , 2015, Environmental microbiology.

[21]  Martin Wu,et al.  A generation‐time effect on the rate of molecular evolution in bacteria , 2015, Evolution; international journal of organic evolution.

[22]  E. Marañón.  Cell size as a key determinant of phytoplankton metabolism and community structure. , 2015, Annual review of marine science.

[23]  U. Riebesell,et al.  Adaptation of a globally important coccolithophore to ocean warming and acidification , 2014 .

[24]  Timothy M. Lenton,et al.  The impact of temperature on marine phytoplankton resource allocation and metabolism , 2013 .

[25]  K. Gao,et al.  EVOLUTIONARY RESPONSES OF A COCCOLITHOPHORID GEPHYROCAPSA OCEANICA TO OCEAN ACIDIFICATION , 2013, Evolution; international journal of organic evolution.

[26]  C. Brownlee,et al.  Dissecting the impact of CO2 and pH on the mechanisms of photosynthesis and calcification in the coccolithophore Emiliania huxleyi. , 2013, The New phytologist.

[27]  M. Steinke,et al.  Interacting effects of ocean acidification and warming on growth and DMS‐production in the haptophyte coccolithophore Emiliania huxleyi , 2013, Global change biology.

[28]  Elena Litchman,et al.  A Global Pattern of Thermal Adaptation in Marine Phytoplankton , 2012, Science.

[29]  K. Gao,et al.  Photosynthetic responses of Emiliania huxleyi to UV radiation and elevated temperature: roles of calcified coccoliths , 2011 .

[30]  G. Somero,et al.  The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’ , 2010, Journal of Experimental Biology.

[31]  A. Lopez-Urrutia,et al.  Increasing importance of small phytoplankton in a warmer ocean , 2010 .

[32]  Aaron Christ,et al.  Mixed Effects Models and Extensions in Ecology with R , 2009 .

[33]  A. Zuur,et al.  Mixed Effects Models and Extensions in Ecology with R , 2009 .

[34]  Fei-xue Fu,et al.  Interactive effects of increased pCO2, temperature and irradiance on the marine coccolithophore Emiliania huxleyi (Prymnesiophyceae) , 2008 .

[35]  Elena Litchman,et al.  The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem level. , 2007, Ecology letters.

[36]  Alan Y. Chiang,et al.  Generalized Additive Models: An Introduction With R , 2007, Technometrics.

[37]  W. Balch,et al.  Prediction of pelagic calcification rates using satellite measurements , 2007 .

[38]  W. Balch,et al.  Relating coccolithophore calcification rates to phytoplankton community dynamics: Regional differences and implications for carbon export , 2007 .

[39]  R. Geider,et al.  ELEVATED ATMOSPHERIC CARBON DIOXIDE INCREASES ORGANIC CARBON FIXATION BY EMILIANIA HUXLEYI (HAPTOPHYTA), UNDER NUTRIENT‐LIMITED HIGH‐LIGHT CONDITIONS 1 , 2005 .

[40]  Geoffrey B. West,et al.  Effects of Body Size and Temperature on Population Growth , 2004, The American Naturalist.

[41]  A. Broerse,et al.  Life-cycle associations involving pairs of holococcolithophorid species: intraspecific variation or cryptic speciation? , 2002 .

[42]  E. Paasche.  A review of the coccolithophorid Emiliania huxleyi (Prymnesiophyceae), with particular reference to growth, coccolith formation, and calcification-photosynthesis interactions , 2001 .

[43]  James H. Brown,et al.  UNM Digital Repository UNM Digital Repository Effects of size and temperature on metabolic rate Effects of size and temperature on metabolic rate , 2022 .

[44]  V. Carey,et al.  Mixed-Effects Models in S and S-Plus , 2001 .

[45]  E. Paasche.  Reduced coccolith calcite production under light-limited growth: a comparative study of three clones of Emiliania huxleyi (Prymnesiophyceae) , 1999 .

[46]  E. Paasche,et al.  Growth and calcification in the coccolithophorid Emiliania huxleyi (Haptophyceae) at low salinities , 1996 .

[47]  T. Tyrrell,et al.  Importance of light for the formation of algal blooms by Emiliania huxleyi , 1996 .

[48]  J. Raven,et al.  Temperature and algal growth , 1988 .

[49]  P. Holligan,et al.  Satellite and ship studies of coccolithophore production along a continental shelf edge , 1983, Nature.

[50]  J. Kalff,et al.  SIZE‐DEPENDENT PHOSPHORUS UPTAKE KINETICS AND CELL QUOTA IN PHYTOPLANKTON 1 , 1982 .

[51]  P. Sharpe,et al.  Non-linear regression of biological temperature-dependent rate models based on absolute reaction-rate theory. , 1981, Journal of theoretical biology.

[52]  J. Lund.  Studies on Asterionella: I. The Origin and Nature of the Cells Producing Seasonal Maxima , 1949 .

[53]  J. Atlas,et al.  The Bacteria , 1881, Botanical Gazette.

[54]  K. Gao,et al.  Impacts of UV radiation on photosynthesis and growth of the coccolithophore Emiliania huxleyi (Haptophyceae) , 2010 .

[55]  U. Riebesell,et al.  Coccolithophores and the biological pump: responses to environmental changes , 2004 .

[56]  R. J. Porra,et al.  The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b , 2004, Photosynthesis Research.

[57]  Trevor Platt,et al.  Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton , 1980 .

[58]  J. Strickland,et al.  Sinking rates of marine phytoplankton measured with a fluorometer , 1967 .