Transcriptional patterns of <i>Emiliania huxleyi</i> in the North Pacific Subtropical Gyre reveal the daily rhythms of its metabolic potential

Limón, María D. Hernández; Hennon, Gwenn M. M.; Harke, Matthew J.; Frischkorn, Kyle R.; Haley, Sheean T.; Dyhrman, Sonya T.

doi:10.1111/1462-2920.14855

Cited by 15 publications

(20 citation statements)

References 71 publications

(126 reference statements)

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“…Interestingly, the synthesis of the photosynthetic apparatus always begins a few hours before dawn in our predictions. This behavior is actually observed in several laboratory and field studies, see e.g., [44,20,18]. Microalgae show thus an anticipation capacity -based a priori on their circadian clock [24,36] -which allows them to deal with the day/night cycle optimally according to our assumptions.…”

Section: Optimal Allocation Under Day/night Cyclessupporting

confidence: 61%

“…This reveals that the synthesis of the photosynthetic apparatus begins a few hours before dawn. This behavior is actually observed in several laboratory and field studies [44,20,18], revealing the algal anticipation capacity.…”

Section: Introductionsupporting

confidence: 60%

“…Using our fitted model, optimal allocation strategy under day/night cycles is determined numerically using the direct method with bocop (as done previously in Section 4). In line with [18], we use I max = 1000 µmol.m −2 .s −1 and τ = 0.41 d. Results are presented in Fig. 7.…”

Section: Optimal Allocation Under Day/night Cyclesmentioning

confidence: 99%

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The promise of dawn: Microalgae photoacclimation as an optimal control problem of resource allocation

Mairet

Bayen

2021

Journal of Theoretical Biology

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Photosynthetic microorganisms are known to adjust their photosynthetic capacity according to light intensity. This so-called photoacclimation process may correspond at equilibrium to the optimal behavior in order to maximize growth. But its dynamics under varying condition remains less understood. To tackle this problem, we propose here a resource allocation model, at coarse-grained, to represent microalgae growth and photoacclimation. Using the Pontryagin maximum principle and numerical simulations, we determine the optimal strategy of resource allocation in order to optimize microalgal growth rate over a time horizon. We show that, after a transient, the optimal trajectory approaches the optimal steady state, a behavior known as the turnpike property. Then, the model is fitted with experimental data, resulting in a bi-level optimization problem which is solved numerically. The fitted trajectory represents well a Dunaliella tertiolecta culture facing a light down-shift. Finally, we compute the optimal trajectory under day/night cycle and show that the synthesis of the photosynthetic apparatus starts a few hours before dawn. This anticipatory behavior has actually been observed both in the laboratory and in the field. This shows the algal predictive capacity and the interest of our method which predicts this phenomenon.

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Section: Optimal Allocation Under Day/night Cyclessupporting

confidence: 61%

Section: Introductionsupporting

confidence: 60%

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The promise of dawn: Microalgae photoacclimation as an optimal control problem of resource allocation

Mairet

Bayen

2021

Journal of Theoretical Biology

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“…It may be that there are differences in transporter localization, and affinity with different E. huxleyi NAR and AMT lineages, and this could be the basis for the regulation difference observed here. When comparing field patterns to culture controls differences may also be attributed to other factors including differences in strain‐composition in the field population and variation in the diel period at the time of sampling (Hernández Limón et al ., ). One potential driver of the observed differences is that unlike culture studies done on axenic isolates, these microcosm experiments were performed with whole seawater, consisting of mixed communities of heterotrophic, mixotrophic, and autotrophic organisms.…”

Section: Resultsmentioning

confidence: 97%

Transcriptional response of Emiliania huxleyi under changing nutrient environments in the North Pacific Subtropical Gyre

Alexander

Rouco

Haley

et al. 2020

Environmental Microbiology

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The widespread coccolithophore Emiliania huxleyi is an abundant oceanic phytoplankton, impacting the global cycling of carbon through both photosynthesis and calcification. Here, we examined the transcriptional responses of populations of E. huxleyi in the North Pacific Subtropical Gyre to shifts in the nutrient environment. Using a metatranscriptomic approach, nutrient-amended microcosm studies were used to track the global metabolism of E. huxleyi. The addition of nitrate led to significant changes in transcript abundance for gene pathways involved in nitrogen and phosphorus metabolism, with a decrease in the abundance of genes involved in the acquisition of nitrogen (e.g. N-transporters) and an increase in the abundance of genes associated with phosphate acquisition (e.g. phosphatases). Simultaneously, after the addition of nitrate, genes associated with calcification and genes unique to the diploid life stages of E. huxleyi significantly increased. These results suggest that nitrogen is a major driver of the physiological ecology of E. huxleyi in this system and further suggest that the addition of nitrate drives shifts in the dominant lifestage of the population. Together, these results underscore the importance of phenotypic plasticity to the success of E. huxleyi, a characteristic that likely underpins its ability to thrive across a variety of marine environments. 2−

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“…In the euphotic zone of the ocean, marine phytoplankton exhibit diel patterns in the transcriptional activity that optimize photosynthesis and nutrient uptake [8][9][10][11][12][13][14][15][16][17][18] . In particular, light and nutrient-limitation in the open ocean drive oscillations in critical metabolic processes in bacteria.…”

Section: Introductionmentioning

confidence: 99%

Metabolic Shifts in Marine Phytoplankton From Viral Infection and Diel Cycles Uncovered Using Dynamic Bayesian Networks

Liu¹,

Hurwitz²

2020

Preprint

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Viruses play a fundamental role in the ecological dynamics of marine microbes by influencing host metabolic flux and altering population size via viral lysis. Despite recent advances in understanding the temporal and environmental factors that drive community-level microbial interactions, viral activity is currently unaccounted for in biogeochemical models. Moreover, the host’s metabolic response to viral infection in natural systems remains elusive. Here, we examine changes in metabolism in marine microbial communities related to virus activity and diel cycles in the surface oceans in the North Pacific Subtropical Gyre (NPSG). We use a time-varying dynamic Bayesian network (DBN) to untangle gene co-expression networks in dominant microbes associated with the environment. The resulting data suggest that viruses play a significant role in driving microbial metabolic flux on par with diel cycles. Most notably, viruses play an opportunistic role by synchronizing viral lysis with diel cycles in their photoautotrophic hosts; and continually infecting heterotrophic hosts by co-opting their alternative energy production strategies to drive replication throughout the day. This work provides a unified model that accounts for both viral activity and diel cycles to predict the distribution, variability, and trajectory of dominant microbes and their key metabolic pathways in global ocean processes.

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Transcriptional patterns of Emiliania huxleyi in the North Pacific Subtropical Gyre reveal the daily rhythms of its metabolic potential

Abstract: This is the author manuscript accepted for publication and has undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as

Cited by 15 publications

References 71 publications

The promise of dawn: Microalgae photoacclimation as an optimal control problem of resource allocation

The promise of dawn: Microalgae photoacclimation as an optimal control problem of resource allocation

Transcriptional response of Emiliania huxleyi under changing nutrient environments in the North Pacific Subtropical Gyre

Metabolic Shifts in Marine Phytoplankton From Viral Infection and Diel Cycles Uncovered Using Dynamic Bayesian Networks

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