Diel variability of photosynthetic picoplankton in the equatorial Pacific

Vaulot, Daniel; Marie, Dominique

doi:10.1029/98jc01333

Cited by 205 publications

(205 citation statements)

References 54 publications

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“…To approximate the spatial gradient of C, we assumed that Prochlorococcus abundances remain constant from day to day at a given location, as observed from previous studies (31,32) and during the first day on station (Fig. 2C, from day 1 to day 2).…”

Section: Methodsmentioning

confidence: 99%

Light-driven synchrony of Prochlorococcus growth and mortality in the subtropical Pacific gyre

Ribalet

Swalwell

Clayton

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

133

156

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Theoretical studies predict that competition for limited resources reduces biodiversity to the point of ecological instability, whereas strong predator/prey interactions enhance the number of coexisting species and limit fluctuations in abundances. In open ocean ecosystems, competition for low availability of essential nutrients results in relatively few abundant microbial species. The remarkable stability in overall cell abundance of the dominant photosynthetic cyanobacterium Prochlorococcus is assumed to reflect a simple food web structure strongly controlled by grazers and/or viruses. This hypothesized link between stability and ecological interactions, however, has been difficult to test with open ocean microbes because sampling methods commonly have poor temporal and spatial resolution. Here we use continuous techniques on two different winter-time cruises to show that Prochlorococcus cell production and mortality rates are tightly synchronized to the day/night cycle across the subtropical Pacific Ocean. In warmer waters, we observed harmonic oscillations in cell production and mortality rates, with a peak in mortality rate consistently occurring ∼6 h after the peak in cell production. Essentially no cell mortality was observed during daylight. Our results are best explained as a synchronized two-component trophic interaction with the per-capita rates of Prochlorococcus consumption driven either directly by the day/night cycle or indirectly by Prochlorococcus cell production. Light-driven synchrony of food web dynamics in which most of the newly produced Prochlorococcus cells are consumed each night likely enforces ecosystem stability across vast expanses of the open ocean.cyanobacteria | cell division | mortality | flow cytometry | SeaFlow P otential interdependencies between species diversity and ecosystem stability have gained increased focus due to global changes in species distributions and abundances (1). Strong predator-prey interactions are predicted to enhance the number of coexisting species and limit fluctuations in abundances (2, 3), whereas competition for limited resources is predicted to reduce biodiversity, in some instances, to the point of ecological instability (3, 4). Mechanisms underlying ecosystem stability remain challenging to characterize on relevant temporal and spatial scales, in part because few empirical data are available to test these theories.Our focus is on the microbial communities within surface waters of the vast oligotrophic gyre of the north Pacific Subtropical Ocean. Here, competition for low concentrations of essential nutrients is hypothesized to result in relatively few abundant microbial species, typified by their extremely small cell sizes and streamlined genomes (5). The cyanobacterium Prochlorococcus numerically dominates the photosynthetic community in these regions, with a relatively constant cell abundance close to half a billion cells per liter despite a population doubling time of approximately one day (6). Such constant cell numbers are predicted when both...

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Section: Methodsmentioning

confidence: 99%

Light-driven synchrony of Prochlorococcus growth and mortality in the subtropical Pacific gyre

Ribalet

Swalwell

Clayton

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

133

156

View full text Add to dashboard Cite

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“…A major limitation of this approach is its implicit assumption that (at the population level) cell growth and division are separated in time. Although most cell division occurs around dusk (10,11), these processes have been observed to occur simultaneously throughout the day in cultures of Synechococcus, especially when division rate is high (>0.7 d −1 ) (7,11,12). Under such conditions, this approach underestimates division rate.…”

mentioning

confidence: 90%

“…The increase in cell volume during daylight hours provides a minimum estimate of the daily division rate (8). This approach has been used to study Synechococcus, Prochlorococcus, and picoeukaryotes in the open ocean (8)(9)(10). A major limitation of this approach is its implicit assumption that (at the population level) cell growth and division are separated in time.…”

mentioning

confidence: 99%

Diel size distributions reveal seasonal growth dynamics of a coastal phytoplankter

Hunter-Cevera¹,

Neubert²,

Solow

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Phytoplankton account for roughly half of global primary production; it is vital that we understand the processes that control their abundance. A key process is cell division. We have, however, been unable to estimate division rate in natural populations at the appropriate timescale (hours to days) for extended periods of time (months to years). For phytoplankton, the diel change in cell size distribution is related to division rate, which offers an avenue to obtain estimates from in situ observations. We show that a matrix population model, fit to hourly cell size distributions, accurately estimates division rates of both cultured and natural populations of Synechococcus. Application of the model to Synechococcus at the Martha's Vineyard Coastal Observatory provides an unprecedented view that reveals a distinct seasonality in division rates. This information allows us to separate the effects of growth and loss quantitatively over an entire seasonal cycle. We find that division and loss processes are tightly coupled throughout the year. The large seasonal changes in cell abundance are the result of periods of time (weeks to months) when there are small systematic differences that favor either net growth or loss. We also find that temperature plays a critical role in limiting division rate during the annual spring bloom. This approach opens a path to quantify the role of Synechococcus in ecological and biogeochemical processes in natural systems.flow cytometry | phytoplankton blooms | FlowCytobot | cyanobacteria M arine phytoplankton contribute ∼50% of global net primary production (1), mediate global biogeochemical cycles, and form the base of marine food webs. It is vital that we understand the factors that govern their abundance, even more so in light of ongoing climate change. The key to this is an understanding of the rate at which phytoplankton cells divide under different environmental conditions. Division rate cannot be measured from changes in cell abundance alone, as changes in abundance result from interactions between cell division and other processes such as predation, advection, sinking, and mixing. Further, we lack approaches that can resolve these processes on scales relevant to the cells' responses to their environment. To overcome this, estimates of abundance and division rate are needed on time scales of hours to days and extending for weeks, months, and ultimately years. Although some progress has been made with automated sampling (2), a practical method for estimating division rates across this wide range of scales has remained elusive. Conventional methods require incubations (3, 4) or sample manipulation and handling (5-7), neither of which can be feasibly conducted at daily resolution for extended duration.For the important class of picophytoplankton (≤2 μm in diameter), estimation of division rates has been attempted from in situ diel changes in cell size. During daylight, individual cells photosynthesize and increase in volume. The increase in cell volume during daylight hours provides a...

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“…A major limitation of this approach is its implicit assumption that (at the population level) cell growth and division are separated in time. While most cell division occurs around dusk [114,111], in fact these processes have been observed to occur simultaneously throughout the day in cultures of Synechococcus, especially when division rate is high (> 0.7 d 1 ) [10,114,42]. Under such conditions, this approach underestimates division rate.…”

Section: Introductionmentioning

confidence: 99%

“…The increase in cell volume during daylight hours provides a minimum estimate of the daily division rate [25]. This approach has been used to study Synechococcus, Prochlorococcus, and picoeukaryotes in the open ocean [25,11,111]. A major limitation of this approach is its implicit assumption that (at the population level) cell growth and division are separated in time.…”

Section: Introductionmentioning

confidence: 99%

Population dynamics and diversity of Synechococcus on the New England Shelf

Hunter-Cevera¹

2014

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Synechococcus is a ubiquitous marine primary producer. Our understanding of the factors that determine its abundance has been limited by available observational tools, which have not been able to resolve population dynamics at timescales that match response times of cells (hours-days). Development of an automated flow cytometer (FlowCytobot) has enabled hourly observation of Synechococcus at the Martha's Vineyard Coastal Observatory (MVCO) since 2003. In order to ascribe changes in cell abundances to either growth or loss processes, information on division rate is needed. I refined a matrix population model that relates diel changes in the distribution of cell volume to division rate and demonstrated that it provides accurate estimates of daily division rate for both cultured and natural populations. Application of the model to the 11-year MVCO time series reveals that division rate is temperature limited during winter and spring, but light limited during fall. Inferred loss rates closely follow division rate in magnitude over the entire seasonal cycle, suggesting that losses are mainly generated by biological processes. While Synechococcus cell abundance, division rate, and loss rate demonstrate striking seasonal patterns, there are also significant shorter timescale variations and important multi-year trends that may be linked to climate. Interpretation of population dynamic patterns is complicated by the diversity found within marine Synechococcus, which is partitioned into 20 genetically distinct clades. Each clade may represent an ecotype, with a distinct ecological niche. To understand how diversity may affect population dynamics, I assessed the diversity at MVCO over annual cycles with culture-independent and dependent approaches. The population at MVCO is diverse, but dominated by clade I representatives throughout the year. Other clades were only found during summer and fall. High through-put sequencing of a diversity marker allowed a more quantitative investigation into these patterns. Five main Synechococcus oligotypes that comprise the population showed seasonal abundance patterns: peaking either during the spring bloom or during late summer and fall. This pattern strongly suggests that features of seasonal abundance are affected by the underlying diversity structure. Synechococcus abundance patterns result from a complex interplay among seasonal environmental changes, diversity, and biological losses.

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Diel variability of photosynthetic picoplankton in the equatorial Pacific

Cited by 205 publications

References 54 publications

Light-driven synchrony of Prochlorococcus growth and mortality in the subtropical Pacific gyre

Light-driven synchrony of Prochlorococcus growth and mortality in the subtropical Pacific gyre

Diel size distributions reveal seasonal growth dynamics of a coastal phytoplankter

Population dynamics and diversity of Synechococcus on the New England Shelf

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