Low Abundances but High Growth Rates of Coastal Heterotrophic Bacteria in the Red Sea

Abstract

Characterized by some of the highest naturally occurring sea surface temperatures, the Red Sea remains unexplored regarding the dynamics of heterotrophic prokaryotes. Over 16 months, we used flow cytometry to characterize the abundance and growth of four physiological groups of heterotrophic bacteria: membrane-intact (Live), high and low nucleic acid content (HNA and LNA) and actively respiring (CTC+) cells in shallow coastal waters. Chlorophyll a, dissolved organic matter (DOC and DON) concentrations, and their fluorescent properties were also measured as proxies of bottom-up control. We performed short-term incubations (6 days) with the whole microbial community (Community treatment), and with the bacterial community only after removing predators by filtration (Filtered treatment). Initial bacterial abundances ranged from 1.46 to 4.80 × 105 cells mL-1. Total specific growth rates in the Filtered treatment ranged from 0.76 to 2.02 d-1. Live and HNA cells displayed similar seasonal patterns, with higher values during late summer and fall (2.13 and 2.33 d-1, respectively) and lower in late spring (1.02 and 1.01 d-1, respectively). LNA cells were outgrown by the other physiological groups (0.33–1.08 d-1) while CTC+ cells (0.28–1.85 d-1) showed weaker seasonality. The Filtered treatment yielded higher bacterial abundances than the Community treatment in all but 2 of the incubations, and carrying capacities peaked in November 2016 (1.04 × 106 cells mL-1), with minimum values (3.61 × 105 cells mL-1) observed in May 2017. The high temperatures experienced from May through October 2016 (33.4 ± 0.4°C) did not constrain the growth of heterotrophic bacteria. Indeed, bacterial growth efficiencies were positively correlated with environmental temperature, reflecting the presence of more labile compounds (high DON concentrations resulting in lower C:N ratios) in summer. The overall high specific growth rates and the consistently higher carrying capacities in the Filtered treatment suggest that strong top-down control by protistan grazers was the likely cause for the low heterotrophic bacteria abundances.

Impact of grazing, resource availability and light on prokaryotic growth and diversity in the oligotrophic surface global ocean

“…Grazing reduction promoted an expected significant increase in prokaryotic growth (Figs 2 and 4), in accordance with the previously suggested bacterial growth top-down control under oligotrophic conditions (Caron et al, 2000;Gasol et al, 2002;Pernthaler, 2005, Silva et al, 2019. Consistent with theoretical models (Thingstad and Lignell, 1997;Thingstad, 2000), experimental data (Richert et al, 2015;Baltar et al, 2016) and field observations (Storesund et al, 2016), grazing appears to have a limited influence on the community composition in our experiments (Figs 5 and 6).…”

“…Depending on the environmental characteristics, microbial communities may be controlled by bottom-up factors (i.e. In oligotrophic waters, it has been suggested that bacterial abundance and production are fundamentally determined by nutrient supply (Sanders et al, 1992), whereas other authors have found that grazing pressure on bacteria is also a relevant regulatory factor (Caron et al, 2000;Gasol et al, 2002;Silva et al, 2019). In oligotrophic waters, it has been suggested that bacterial abundance and production are fundamentally determined by nutrient supply (Sanders et al, 1992), whereas other authors have found that grazing pressure on bacteria is also a relevant regulatory factor (Caron et al, 2000;Gasol et al, 2002;Silva et al, 2019).…”

“…nutrient availability), top-down factors (grazing or viral lysis), as well as by temperature (Sunagawa et al, 2015;Morán et al, 2017) and light Richert et al, 2015 in a changing balance. In oligotrophic waters, it has been suggested that bacterial abundance and production are fundamentally determined by nutrient supply (Sanders et al, 1992), whereas other authors have found that grazing pressure on bacteria is also a relevant regulatory factor (Caron et al, 2000;Gasol et al, 2002;Silva et al, 2019).…”

Responses of physiological groups of tropical heterotrophic bacteria to temperature and dissolved organic matter additions: food matters more than warming

“…Moreover, the physiological structure sensu del Giorgio and Gasol () of tropical and subtropical assemblages has remained largely unexplored. A few individual reports on the distribution of LNA and HNA bacteria (Andrade et al ., ; Andrade et al ., ; Girault et al ., ; Bock et al ., ) and on Live and Dead cells (Gasol et al ., ; Baltar et al ., ) were recently complemented by a study on the annual variability in the abundance and specific growth rates of the same physiological groups assessed here at an equivalent northern latitude in the coastal Red Sea (Silva et al ., ). Although experiments using sudden modifications in environmental conditions and monitored for a few days strongly limit our capability to assess future ecosystem responses, they provide a first and valuable step to set up possible directions of change.…”

“…total abundances), with only a few considering the physiological structure from an individual perspective (Gasol et al ., ; Morán and Calvo‐Díaz, ; Morán et al ., ; Huete‐Stauffer et al ., ). However, rarely have the above‐mentioned physiological groups been jointly assessed in tropical ecosystems (Silva et al ., ).…”