Periodic Reporting for period 1 - Warming calcifiers (Evolutionary processes in calcifying organisms under future warming and biogeochemical implications)
Okres sprawozdawczy: 2021-09-01 do 2023-08-31
Marine calcifiers play essential roles in marine ecosystems including contributing to the marine food web and the marine carbonate pump. A major group of calcifying organisms are coccolithophores that are considered to be the most prominent carbonate producer in the ocean and also contribute about 50% of global primary production. The combination of photosynthesis and calcification makes them highly influential on the ocean-atmosphere CO2 exchange. Moreover, they provide a mechanism for a major component of export of carbon via the sedimentation of their carbonate shells in the deep ocean. Coccolithophores contribute most of the carbonate in deep oligotrophic regions while in shallow-water environments other organisms, such as Large Benthic Foraminifera (LBF) are major carbonate producers. This group is usually characterised by algal symbiosis, making them contributors to primary production in the photic zone of tropical to subtropical areas.
Temperature is a first order control on a large number of their physiological processes including calcification and photosynthesis. Thus, future warming and its influence on calcifying organisms may have a major impact on the modern carbon cycle. An important mechanism that allows organisms to cope with climate change is physiological plasticity within ontogenetic development and across generations.
The primary objective of this study was to explore the adaptation potential to future warming in the two main groups of calcifying organisms and to better understand their biogeochemical implications. The overarching conclusion is that both groups have significant potential for adaptation, which could potentially mitigate the effects of future warming on them. However, this potential is highly dependent on the rate of warming. Further, while photosynthesis could be positively influenced by adaptation to elevated temperatures, the species-specific effects of thermal stress and adaptation on calcification could result in changes to CO2 sink or source behaviours. To accurately quantify these effects, it is necessary to integrate both geochemical and ecological modelling techniques in further research.
Temperature is a first order control on a large number of their physiological processes including calcification and photosynthesis. Thus, future warming and its influence on calcifying organisms may have a major impact on the modern carbon cycle. An important mechanism that allows organisms to cope with climate change is physiological plasticity within ontogenetic development and across generations.
The primary objective of this study was to explore the adaptation potential to future warming in the two main groups of calcifying organisms and to better understand their biogeochemical implications. The overarching conclusion is that both groups have significant potential for adaptation, which could potentially mitigate the effects of future warming on them. However, this potential is highly dependent on the rate of warming. Further, while photosynthesis could be positively influenced by adaptation to elevated temperatures, the species-specific effects of thermal stress and adaptation on calcification could result in changes to CO2 sink or source behaviours. To accurately quantify these effects, it is necessary to integrate both geochemical and ecological modelling techniques in further research.
1)I have characterised the baseline thermal tolerance of nine strains of Emiliania huxleyi, a dominant member of the coccolithophores group with a wide geographical distribution, that provides an opportunity to explore the effect of local adaptations on thermal tolerance. I examined strains representing polar, temperate, and sub-tropical origins. My results show that their biogeographical origin does not directly affect thermal tolerance, as no clear patterns are created by local adaptation of “cold-adapted”, “moderately-adapted”, and “warm-adapted” strains. Moreover, while all strains exhibit optimal growth at 23C-25C, the greatest difference in thermal response is observed between Mediterranean strains, suggesting that other factors such as seasonality might play a larger role in local thermal adaptation compared to latitudinal niche partitioning. A growth threshold was identified between 25C-28C for the majority of strains, with the exception of one strain that grew at 28C, albeit slower than in optimal conditions, and one strain exhibiting its threshold between 23C-25C. These results also show similar performance of calcification and photosynthesis across the range of temperatures in which the strains survive and grow.
2)I have characterised the baseline thermal tolerance of a highly and a moderately tolerant large benthic foraminifera (LBF) species between 25C -37C. Both species survived all treatments, but only the resilient species remained functional and continued to calcify at both 35C and 37C as well as maintained positive net photosynthesis.
3)I conducted adaptation experiments on the nine strains of E. huxleyi that were previously adapted to 15C and exposed them to optimal and stress temperatures and documented that the “moderately-adapted” and “warm-adapted” strains have increased their thermal range for survival to include 28C while the “cold- adapted” strains remained limited to 25C. Measurements of photosynthesis rates indicated that adaptation to optimal temperatures increased net photosynthesis under 25C but not under 28C, and exposure to 28C had a neutral or negative effect on photosynthesis. Quantification of calcification rates revealed that adaptation to both optimal and stressful temperatures affected differently among the different strains in varying magnitude.
4)I also conducted proteomics analysis of one strain from the multigenerational experiment aiming to pinpoint the cellular mechanism facilitating thermal adaptation. The strain was chosen as it was the only one that initially survived at 28°C. The analysis showed that following adaptation to the stressful temperature no significant alteration in abundance of any identified protein was significant when comparing cultures grown at 25°C and 28°C. This finding indicates that during the adaptation period, E. huxleyi has been able to overcome the significant alterations to cell functioning recognised under acute exposure to heat stress, modifying its cellular proteome such that temperature-dependent alterations in protein abundance are not detected. Such findings highlight the importance of adaptation in the response to long-term ocean warming. This unplanned work is directly relevant to understanding adaptation in photo-calcifying organisms and provides insight towards the mechanism related to adaptation. This is currently being summarised in a publication and it has also contributed to my training, expanding my skill set with proteomics data analysis.
5)Experiments to examine the role of symbionts in the thermal tolerance of LBF demonstrated they can adapt to elevated temperatures by ‘symbiont switching’ and not by ‘symbiont shuffling’ (as previously suggested). This is important as the symbionts have a much higher reproduction rate enabling faster adaptation which provides a potential mechanism for adaptation of this group.
6)The results from the coccolithophores experiment described in (3) that quantified the changes in calcification and photosynthesis before and after adaptation, demonstrated that the response to adaptation is species-specific but does not follow categories of ‘cold- adapted’ or ‘warm-adapted’ groups. For some strains the critical ratio between photosynthesis and calcification will change the role of coccolithophores to sink while in others they become source for atmospheric CO2. This species-specific response means that to model the biogeochemical impact of changes in pCO2 integration of future species distribution models is required.
Exploitation and dissemination:
The first part of these results, characterisation of the baseline thermal tolerance of E. huxleyi demonstrated that biogeographical origin does not directly affect thermal tolerance, was presented at The Micropalaeontological Society's Annual Meeting in 2022.The paper describing the role of symbionts in the thermal tolerance of LBF through 'symbiont switching' and 'symbiont shuffling' mechanisms is under review, and the remainder of the work is in the process of preparation for additional publications
2)I have characterised the baseline thermal tolerance of a highly and a moderately tolerant large benthic foraminifera (LBF) species between 25C -37C. Both species survived all treatments, but only the resilient species remained functional and continued to calcify at both 35C and 37C as well as maintained positive net photosynthesis.
3)I conducted adaptation experiments on the nine strains of E. huxleyi that were previously adapted to 15C and exposed them to optimal and stress temperatures and documented that the “moderately-adapted” and “warm-adapted” strains have increased their thermal range for survival to include 28C while the “cold- adapted” strains remained limited to 25C. Measurements of photosynthesis rates indicated that adaptation to optimal temperatures increased net photosynthesis under 25C but not under 28C, and exposure to 28C had a neutral or negative effect on photosynthesis. Quantification of calcification rates revealed that adaptation to both optimal and stressful temperatures affected differently among the different strains in varying magnitude.
4)I also conducted proteomics analysis of one strain from the multigenerational experiment aiming to pinpoint the cellular mechanism facilitating thermal adaptation. The strain was chosen as it was the only one that initially survived at 28°C. The analysis showed that following adaptation to the stressful temperature no significant alteration in abundance of any identified protein was significant when comparing cultures grown at 25°C and 28°C. This finding indicates that during the adaptation period, E. huxleyi has been able to overcome the significant alterations to cell functioning recognised under acute exposure to heat stress, modifying its cellular proteome such that temperature-dependent alterations in protein abundance are not detected. Such findings highlight the importance of adaptation in the response to long-term ocean warming. This unplanned work is directly relevant to understanding adaptation in photo-calcifying organisms and provides insight towards the mechanism related to adaptation. This is currently being summarised in a publication and it has also contributed to my training, expanding my skill set with proteomics data analysis.
5)Experiments to examine the role of symbionts in the thermal tolerance of LBF demonstrated they can adapt to elevated temperatures by ‘symbiont switching’ and not by ‘symbiont shuffling’ (as previously suggested). This is important as the symbionts have a much higher reproduction rate enabling faster adaptation which provides a potential mechanism for adaptation of this group.
6)The results from the coccolithophores experiment described in (3) that quantified the changes in calcification and photosynthesis before and after adaptation, demonstrated that the response to adaptation is species-specific but does not follow categories of ‘cold- adapted’ or ‘warm-adapted’ groups. For some strains the critical ratio between photosynthesis and calcification will change the role of coccolithophores to sink while in others they become source for atmospheric CO2. This species-specific response means that to model the biogeochemical impact of changes in pCO2 integration of future species distribution models is required.
Exploitation and dissemination:
The first part of these results, characterisation of the baseline thermal tolerance of E. huxleyi demonstrated that biogeographical origin does not directly affect thermal tolerance, was presented at The Micropalaeontological Society's Annual Meeting in 2022.The paper describing the role of symbionts in the thermal tolerance of LBF through 'symbiont switching' and 'symbiont shuffling' mechanisms is under review, and the remainder of the work is in the process of preparation for additional publications
This study has characterised the adaptation of two groups of calcifying organisms to future warming. Additional publications are currently being prepared to complete the dissemination of the results.