Differential Assimilation of Inorganic Carbon and Leucine by Prochlorococcus in the Oligotrophic North Pacific Subtropical Gyre

Abstract

The light effect on photoheterotrophic processes in Prochlorococcus, and primary and bacterial productivity in the oligotrophic North Pacific Subtropical Gyre was investigated using 14C-bicarbonate and 3H-leucine. Light and dark incubation experiments were conducted in situ throughout the euphotic zone (0–175 m) on nine expeditions to Station ALOHA over a 3-year period. Photosynthetrons were also used to elucidate rate responses in leucine and inorganic carbon assimilation as a function of light intensity. Taxonomic group and cell-specific rates were assessed using flow cytometric sorting. The light:dark assimilation rate ratios of leucine in the top 150 m were ∼7:1 for Prochlorococcus, whereas the light:dark ratios for the non-pigmented bacteria (NPB) were not significant different from 1:1. Prochlorococcus assimilated leucine in the dark at per cell rates similar to the NPB, with a contribution to the total community bacterial production, integrated over the euphotic zone, of approximately 20% in the dark and 60% in the light. Depth-resolved primary productivity and leucine incorporation showed that the ratio of Prochlorococcus leucine:primary production peaked at 100 m then declined steeply below the deep chlorophyll maximum (DCM). The photosynthetron experiments revealed that, for Prochlorococcus at the DCM, the saturating irradiance (Ek) for leucine incorporation was reached at approximately half the light intensity required for light saturation of 14C-bicarbonate assimilation. Additionally, high and low red fluorescing Prochlorococcus populations (HRF and LRF), co-occurring at the DCM, had similar Ek values for their respective substrates, however, maximum assimilation rates, for both leucine and inorganic carbon, were two times greater for HRF cells. Our results show that Prochlorococcus contributes significantly to bacterial production estimates using 3H-leucine, whether or not the incubations are conducted in the dark or light, and this should be considered when making assessments of bacterial production in marine environments where Prochlorococcus is present. Furthermore, Prochlorococcus primary productivity showed rate to light-flux patterns that were different from its light enhanced leucine incorporation. This decoupling from autotrophic growth may indicate a separate light stimulated mechanism for leucine acquisition.

Temporal and vertical variability in picophytoplankton primary productivity in the North Pacific Subtropical Gyre

“…Consistent with the numerical dominance and estimated carbon biomass of Prochlorococcus, these organisms contributed > 60% to the total sorted picophytoplankton productivity (equaling ~39% of total > 0.2 µm filter-based productivity), which agrees with previously reported measurements at Station ALOHA (Björkman et al 2015). In contrast to Prochlorococcus, PPE cell abundances were orders of magnitude lower; however, PPE contributed up to 36% to sorted picophytoplankton production and biomass (equivalent to ~11% to total filter-based productivity).…”

“…Amongst the picophytoplankton, cellular abundances of Pro chloro coccus are typically orders of magnitude greater than those of Synechococcus or PPE in the NPSG, and past studies have largely focused on understanding the controls on cyanobacterial growth rather than their eukaryotic counterparts (e.g. Campbell & Vaulot 1993, Campbell et al 1994, Liu et al 1995, Björkman et al 2015. However, studies from the subtropical Atlantic Ocean have reported high cell-specific rates of 14 C primary production by PPE, making them potentially significant contributors to carbon fixation (Li 1994, Jardillier et al 2010.…”

“…In addition, studies have characterized the specific contributions of picoplankton assemblages to rates of primary production through particle size distributions , specific photosynthetic pigment-based labeling (Goericke & Welschmeyer 1993, Pinckney et al 1996, and flow cytometric sorting of radiolabeled cells (Li 1994, Jardillier et al 2010, Björkman et al 2015, Rii et al 2016). In the current study, we relied on combined size-fractionated measurements of 14 C-bicarbonate assimilation and flow cytometric sorting of 14 Clabeled picoplankton populations to examine vertical and temporal patterns in carbon fixation on 11 cruises to Station ALOHA spanning a 1 yr period.…”

Mixotrophic metabolism by natural communities of unicellular cyanobacteria in the western tropical South Pacific Ocean

“…Yet, recent evidence has shown that the uptake of organic N‐ (leucine, amino acids) and P‐ (ATP) molecules by Prochlorococcus and Synechococcus is enhanced in the light (Michelou et al ., ; Mary et al ., ; Duhamel et al ., ; Gómez‐Pereira et al ., ). Therefore, previous studies (e.g., Zubkov et al ., ; Michelou et al ., ; Zubkov, ; Gómez‐Pereira et al ., ; Moore, ; Muñoz‐Marín et al ., ; Björkman et al ., ) since the early work of Rippka () have commonly defined this nutritional plasticity in marine cyanobacteria as photoheterotrophy, although sensus stricto this term defines organisms that use light for energy, but cannot use CO 2 as their sole C source. However, these studies demonstrating light‐enhancement of N or P‐containing organic molecules uptake did not directly verify if marine cyanobacteria could also use organic molecules containing only C (e.g., glucose) and if light also enhances organic C assimilation.…”

Dynamics of Prochlorococcus and Synechococcus at Station ALOHA Revealed through Flow Cytometry and High-Resolution Vertical Sampling

“…The inhabitants of the pycnocline are not always in the dark but may experience elevated light conditions of an aperiodic, random nature due to subsurface waves. If there are differences in genomic traits between mixedlayer and pycnocline inhabitants, they can be expected to include metabolic requirements (Björkman et al, 2015) and adaptations to a diel light cycle in the mixed-layer zone vs. a random irradiance regime in the pycnocline (Ottesen et al, 2014).…”