Diel dynamics and coupling of heterotrophic prokaryotes and dissolved organic matter in epipelagic and mesopelagic waters of the central Red Sea

Abstract

The ecological status of an ecosystem can be approached by the taxa present but also by the size of individual organisms. In aquatic ecosystems, flow cytometry (FC) allows to study the individual size spectra and broad community composition through the evaluation of cytometric categories. The Red Sea represents a warm oligotrophic environment with a strong diel signal of vertically migrating mesopelagic fish, which feed at night at the surface and release dissolved organic carbon (DOC) at depth during day-time. However, knowledge about how these conditions affect the dynamics of heterotrophic prokaryotes (HP) and their coupling with DOC is lacking. Here, we analyzed a high frequency sampling over 24 h to identify the community structure and compositional changes of HP in the epipelagic and mesopelagic layers of the central Red Sea. Our results show marked vertical and diel changes in HP communities in both layers. Specifically, the relative contribution of high nucleic acid content cells was remarkably linked to changes in DOC concentration and properties. The patterns observed were likely associated to the diel vertical migration of mesopelagic fish. These findings reveal that the structure of microbial communities in warm oligotrophic environments may be more dynamic than previously thought.

Peer Review #3 of "Seasonal variability and vertical distribution of autotrophic and heterotrophic picoplankton in the Central Red Sea (v0.1)"

“…Regarding the vertical distribution of heterotrophic prokaryotes, we confirm the findings of two recent studies conducted at the same site as ours, focused on the interactions of bacteria with DOC stocks at the diel (García et al 2018) and seasonal scales (Calleja et al 2019). As previously reported (Calleja et al 2019;García et al 2018), LNA bacteria dominated in the epipelagic zone while HNA bacteria prevailed in the mesopelagic zone.…”

“…For heterotrophic prokaryotes, although our knowledge about their diversity is increasing (Ngugi et al 2012;Pearman et al 2017;Thompson et al 2017), only a few studies have investigated their vertical distribution in Red Sea waters (Calbet et al 2015;Qian et al 2011). A recent report using data collected from the same site as this study has shown that the abundance of heterotrophic bacteria can change temporally up to 3-fold within the same depth in the upper epipelagic (Calleja et al 2019;García et al 2018). Other studies conducted at that site have shown that LNA bacteria dominated in the epipelagic layer, while HNA cells were more abundant in the mesopelagic layer, indicating that each group seems to prefer different environmental conditions Calleja et al 2018).…”

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

“…), and in tropical waters in general (Morán et al 2017). However, likewise early observations in the Caribbean (Johnson et al 1981) recently confirmed for this site (García et al 2018), DOM concentrations displayed a coherent diel pattern suggesting different timing of production and consumption ( Fig. 1 ).…”

“…Heterotrophic prokaryotes inhabiting the Red Sea seem to challenge this view. Together with diel variations of standing stocks (García et al 2018), this study), night- and day-initiated incubations of predator-free ambient assemblages with the DOM pool available at the time of sampling yielded surprising similarities in epipelagic and mesopelagic waters. A method for estimating division rates in cyanobacteria based in changes in cell size (Hunter-Cevera et al 2014, Sosik et al 2003) was adapted to obtain independent estimates of in situ net growth rates ( Fig.…”

“…DVM fishes have been recently suggested to generate hotspots for heterotrophic prokaryotes, yielding significantly higher bacterial growth efficiencies compared with shallower layers (Calleja et al 2018). An analysis of a 24 h intensive sampling at the same location has supported the existence of diel inputs of labile DOM fueling the HP community at the depths occupied by mesopelagic fishes during daytime (García et al 2018). Both DOC concentrations and the contribution of high nucleic acid content (HNA) bacteria, usually made up of copiotrophic taxa (Schattenhofer et al 2011, Vila-Costa et al 2012) more active than the low nucleic acid content (LNA) group (e.g.…”