Diel dynamics of dissolved organic matter and heterotrophic prokaryotes reveal enhanced growth at the ocean's mesopelagic fish layer during daytime

Morán, Xosé Anxelu G.; García, Francisca C.; Røstad, Anders; Silva, Luis; Al-Otaibi, Najwa; Irigoien, Xabier; Calleja, María Ll.

doi:10.1016/j.scitotenv.2021.150098

Cited by 14 publications

(9 citation statements)

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“…The deep scattering layer (DSL), located between 400 and 600 m at our study site (Klevjer et al, 2016), is dominated by Benthosema pterotum lanternfishes. The labile dissolved organic matter released by the fishes fuels an active community of heterotrophic prokaryotes at the DSL (Calleja et al, 2018;García et al, 2018), with significant differences between day and night linked to the presence and absence, respectively, of mesopelagic fish (Morán et al, 2022). Our LNA and HNA prokaryotes specific growth rate estimates did not show any consistent increase at the DSL depth (Figure 6).…”

Section: Discussionmentioning

confidence: 80%

“…Our LNA and HNA prokaryotes specific growth rate estimates did not show any consistent increase at the DSL depth (Figure 6). Although in direct incubations Calleja et al (2018) had reported higher specific growth rates of heterotrophic prokaryotes from mesopelagic depths than those at the surface, a more recent study using the same approach found the opposite (Morán et al, 2022), indicating that vertical variations in their growth rates can also vary temporally, especially for the HNA group (see for instance Winter values in Figure 6B).…”

Section: Discussionmentioning

confidence: 88%

“…Unfortunately, this was the only concurrent autotrophic and heterotrophic picoplankton growth rate experiment conducted at the study site but given the high percentage of variance explained we felt it was safe to extrapolate this relationship to the remaining periods. Two additional experiments focused on heterotrophic prokaryotes and how migrating mesopelagic fishes were able to supply labile DOC to sustain their growth rate (Calleja et al, 2018;Morán et al, 2022) were not included because no information about picophytoplankton was available. Previous studies have estimated in situ division rates of picoplankton populations from the ratio of the maximum to the minimum flow cytometric right angle light scatter value, a common proxy for picoplankton cell size (Vaulot and Marie, 1999;Jacquet et al, 2002;Lefort and Gasol, 2014).…”

Section: Discussionmentioning

confidence: 99%

“…During the winter sampling, 10 L seawater was collected from the surface (5 m) and from 550 m depth (i.e., the depth with the strongest acoustic signal of the deep scattering layer formed by mesopelagic fish during light hours, Calleja et al, 2018;Morán et al, 2022) at midnight (Supplementary Figure 1B). Water was pre-filtered through pre-combusted Whatman GF/C filters (1.2 µm) in order to remove protistan grazers.…”

Section: Experimental Incubations For Estimating Specific Growth Rates From Cell Size Changesmentioning

confidence: 99%

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Picoplankton Diel Variability and Estimated Growth Rates in Epipelagic and Mesopelagic Waters of the Central Red Sea

2021

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The diel variability of the abundance and cell size of picoplanktonic groups in the central Red Sea was monitored every 2 h in situ on 4 occasions (once per season) from 2015 to 2016. We distinguished Prochlorococcus, low (LF-Syn) and high (HF-Syn) fluorescence Synechococcus, small (Speuk) and large (Lpeuk) picoeukaryotes and two groups of heterotrophic prokaryotes of low (LNA) and high (HNA) nucleic acid content. The diel variability in abundance was less marked than in cell size and more apparent in autotrophs than heterotrophs. Specific growth rates were estimated by an empirical relationship from measurements obtained in bottle incubations of surface and deep samples collected in the winter compared with in situ variations in cell size over 24 h. Autotrophic picoplankton groups generally grew faster (0.23–0.77 d–1) than heterotrophic prokaryotes (0.12–0.50 d–1). Surface to 100 m depth-weighted specific growth rates displayed a clear seasonal pattern for Prochlorococcus, with maxima in winter (0.77 ± 0.07 d–1) and minima in fall (0.52 ± 0.07 d–1). The two groups of Synechococcus peaked in spring, with slightly higher growth rates of LF-Syn (0.57 ± 0.04 d–1) than HF-Syn (0.43 ± 0.04 d–1). Speuk and Lpeuk showed different seasonal patterns, with lower values of the former (0.27 ± 0.02 and 0.37 ± 0.04 d–1, respectively). HNA consistently outgrew LNA heterotrophic prokaryotes, with a higher growth in the epipelagic (0–200 m, 0.36 ± 0.03 d–1) than in the mesopelagic (200–700 m, 0.26 ± 0.03 d–1), while no differences were found for LNA cells (0.19 ± 0.03 d–1 and 0.17 ± 0.02 d–1, respectively). With all data pooled, the mean diel abundances of autotrophic picoplankton in the upper epipelagic and of HNA cells in the epipelagic and mesopelagic layers were significantly correlated with the specific growth rates estimated from cell size variations. Our high-resolution sampling dataset suggests that changes in growth rates underlie the noticeable seasonality of picoplankton recently described in these tropical waters.

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Section: Discussionmentioning

confidence: 80%

Section: Discussionmentioning

confidence: 88%

Section: Discussionmentioning

confidence: 99%

Section: Experimental Incubations For Estimating Specific Growth Rates From Cell Size Changesmentioning

confidence: 99%

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Picoplankton Diel Variability and Estimated Growth Rates in Epipelagic and Mesopelagic Waters of the Central Red Sea

2021

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“…The importance of DOM composition in determining BGE is evidenced by the highly consistent consumption of the FDOM protein-like component C4 (consumed in 92% of the incubations, Supplementary Figure 4A ) and the positive correlation of BGE with its initial fluorescence and consumption rate. There is mounting evidence that fluorescent protein-like substances are being selectively taken up by heterotrophic prokaryotes throughout the entire water column of the central Red Sea, fostering their growth ( Silva et al, 2019 ; Morán et al, 2022 ).…”

Section: Discussionmentioning

confidence: 99%

Heterotrophic Bacterioplankton Growth and Physiological Properties in Red Sea Tropical Shallow Ecosystems With Different Dissolved Organic Matter Sources

et al. 2022

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Despite the key role of heterotrophic bacterioplankton in the biogeochemistry of tropical coastal waters, their dynamics have been poorly investigated in relation to the different dissolved organic matter (DOM) pools usually available. In this study we conducted four seasonal incubations of unfiltered and predator-free seawater (Community and Filtered treatment, respectively) at three Red Sea coastal sites characterized by different dominant DOM sources: Seagrass, Mangrove, and Phytoplankton. Bacterial abundance, growth and physiological status were assessed by flow cytometry and community composition by 16S rRNA gene amplicons. The Seagrass site showed the highest initial abundances (6.93 ± 0.30 × 105 cells mL–1), coincident with maximum DOC concentrations (>100 μmol C L–1), while growth rates peaked at the Mangrove site (1.11 ± 0.09 d–1) and were consistently higher in the Filtered treatment. The ratio between the Filtered and Community maximum bacterial abundance (a proxy for top-down control by protistan grazers) showed minimum values at the Seagrass site (1.05 ± 0.05) and maximum at the Phytoplankton site (1.24 ± 0.30), suggesting protistan grazing was higher in open waters, especially in the first half of the year. Since the Mangrove and Seagrass sites shared a similar bacterial diversity, the unexpected lack of bacterial response to predators removal at the latter site should be explained by differences in DOM characteristics. Nitrogen-rich DOM and fluorescent protein-like components were significantly associated with enhanced specific growth rates along the inshore-offshore gradient. Our study confirms the hypotheses that top–down factors control bacterial standing stocks while specific growth rates are bottom-up controlled in representative Red Sea shallow, oligotrophic ecosystems.

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Tracing DOM in the ocean with UV-visible spectroscopy

Stedmon,

Yamashita

2024

Biogeochemistry of Marine Dissolved Organic Matter

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Diel dynamics of dissolved organic matter and heterotrophic prokaryotes reveal enhanced growth at the ocean's mesopelagic fish layer during daytime

Cited by 14 publications

References 77 publications

Picoplankton Diel Variability and Estimated Growth Rates in Epipelagic and Mesopelagic Waters of the Central Red Sea

Picoplankton Diel Variability and Estimated Growth Rates in Epipelagic and Mesopelagic Waters of the Central Red Sea

Heterotrophic Bacterioplankton Growth and Physiological Properties in Red Sea Tropical Shallow Ecosystems With Different Dissolved Organic Matter Sources

Tracing DOM in the ocean with UV-visible spectroscopy

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