1 Phytoplankton adaptation in contrasting aquatic light regimesDavid Talmy, Jerry Blackford, Nick Hardman-Mountford, Luca Polimene, Richard Geider, Chris Hill and Mick Follows

2 Overarching questionsHow much carbon is associated with each unit of chlorophyll? What is the chlorophyll doing? i.e. how much photosynthesis? Derived from SeaWiFS data. Source: NASA Main causes of variation in chl:C and photosynthesis nutrients temperature light

3 Cellular chlorophyll content varies within and between taxaOstreococcus (Six et al., 2008) Thalassiosira peudonana (Geider et al., 1997)

4 A note on photosynthesis-irradiance curves2) Short term incubation experiments X X X 1) Acclimation to given light intensity X photosynthesis X X irradiance 3) Photosynthesis-irradiance relationship

5 Skeletonema Costatum (Anning et al., 2000)Prochlorococcus (Moore et al., 1999)

6 Adaptation vs. acclimation(photo)adaptation: an outcome of evolution as recorded in the gene pool of a species (photo)acclimation: changes in macromolecular composition in response to environmental variation Variation is acclimation, within limits set by adaptation How does variation in chl:C and photosynthetic rate happen as a consequence of adaptation to different environments?

7 Rationale Environment Model cell TraitsEcosystem model / primary production algorithm

8 Environment Cell modelVertical transport influences light variability 1) Light harvesting 2) Carbon fixation CO2 3) Biosynthesis Nutrients Talmy, 2013; adapted from Ross et al. 2008

9 Plants have to allocate resources to machinery for growth and reproduction(Tilman 1990)

10 Phytoplankton cell schematic - Shuter (1979)

11 Mechanistic constraints on photosynthesis and growthX Chemical energy (ATP) and reductant (NADPH) for metabolism Photoprotection Light harvesting

12 Mechanistic constraints on photosynthesis and growthBiosynthesis Light harvesting Carbon fixation Carbon storage Cells are able to accumulate carbon storage compounds in the light, and draw upon those reserves in the dark ‘thin’ ‘fat’ Ross and Geider 2009

13 Model cell Protein is partitioned between each cellular component

14 Cellular nitrogen is a suitable proxy for protein (Geider and La Roche, 2002)

15 Contrasting light regimes“Static” regime Analogous to relatively stable environments, e.g. laboratories, or oligotrophic gyres “Dynamic” regime Analogous to a well-mixed layer Different resource allocation strategies optimize growth?

16 “Dynamic” regime Single cell undergoing naïve diffusion using a random walk model (Kτ= s-1) Depth/irradiance profiles for 10,000 cells all undergoing naïve diffusion

17 Probability mass functions (PMFs) of light exposureIntegrated light dose (ILD) can be altered by varying the optical depth of the mixed layer

18 Assumptions Cells optimise growth in either completely “static”, or completely “dynamic” environments Cells are nutrient replete, light limited Cells allocate resources to maximise growth within a 24 hour photoperiod

19 A genetic algorithm was used to determine solutions:

20 Results Biosynthesis Photoprotection Optimal resource allocations are different in static/dynamic environments Talmy et al. Limnology and Oceanography, 2013

21 Objective: use model predictions of resource allocation to predict photoacclimation strategiesLight harvesting ??? ???

22 Static  ProchlorococcusFlombaum et al, 2013 Static  Prochlorococcus

23 Alvain et al, 2013 dynamic  Diatoms

24 Plasticity of chlorophyll synthesis in organisms optimised to contrasting environments:Static Dynamic Minimums all normalised to unity Moore et al., 1995 Geider et al., 1997 RSS (static) RSS (dynamic) 0.0 0.1 0.5 P. marinus 3.1 2.7 2.4 6.8 34.8 47.8 T.pseudonana 32.4 28.3 27.7 17.5 0.6 2.1

25 “static” “dynamic” Continuum of strategies in between Minimums all normalised to unity Talmy et al. Limnology and Oceanography, 2013

26 A note on photosynthesis-irradiance curves2) Short term incubation experiments X X X 1) Acclimation to given light intensity X photosynthesis X X irradiance 3) Photosynthesis-irradiance relationship

27 Which resource allocation strategy predicts P-I response of Skeletonema Costatum?x x x x x x Anning et al. (2000)

28 Photosynthesis-irradiance response of Skeletonema Costatum (diatom)Dynamic Static Carbon fixation Photoprotection Model predictions Low light acclimated Skeletonema Costatum (Anning et al., 2000) High light acclimated Skeletonema Costatum ● ○ …dynamic optimisation is a better constraint on P-I response in Skeletonema Costatum

29 Photosynthesis-irradiance response of ProchlorococcusP-I response is different for cells optimised to static and dynamic environments (low integrated light dose) Prochloroccus, P-I response is photoinhibited at high irradiance (Moore et al., 1999) static optimisation is a better predictor of (normalised) photosynthesis-irradiance response in high and low light adapted Prochlorococcus Talmy et al. Limnology and Oceanography, 2013

30 Model Data ◦ Saturation point of photosynthesisEk,modelled > growth irradiance Ek,in situ > growth irradiance ◦ ~1-to-1 relationship. ~1-to-1 relationship. (Moore et. al 2006)

31 Conclusions Optimal resource allocations in a `static’ environment show traits similar to organisms adapted to more stable conditions (e.g. Prochlorococcus) In contrast, resource allocations optimal in a dynamic environment are consistent with organisms adapted to rapid mixing (e.g. diatoms). Traits optimal in dynamic / static environments persist, even when cells are cultured in a constant environment

32 How much carbon is associated with each unit of chlorophyll?What is the chlorophyll doing? i.e. how much photosynthesis? Derived from SeaWiFS data. Source: NASA Understanding adaptation allows traits to be meaningfully constrained, without unreasonable complication

33 Use more realistic environments to understand adaptationBackhaus et al., 1999 High res. MITgcm, Aghulas region

34 Future work High resolution MITgcm in the Agulhas with Lagrangian floats to track individual trajectories: Can we parameterize light variability and associated traits?

35 Cells placed in the dark after day 1- Berges and Falkowski 1998 Cells remain photosynthetically capable throughout the experiment

36 Carbon Store Large cell Small cell Photosynthesis Biosynthesis

37 When deeply mixed, small cells run out of carbon reserves

38 Variable C:N ratios during bloom formationKoertzinger et al (2001)

39 …Maybe also explain how primary productivity occurs in winter mixed layers, e.g. In the North Atlantic: r – ‘net specific growth rate’ Chl a (mg m-3) Backhaus et al., 2003 Behrenfeld 2010

40 A note on photosynthesis-irradiance curvesGrowth irradiance curve for many acclimation irradiances Different acclimation irradiances lead to different P-I curves Synechococcus, Kana and Gilbert 1987