Temperature sensitivities of microbial plankton net growth rates are seasonally coherent and linked to nutrient availability

Abstract

Recent work suggests that temperature effects on marine heterotrophic bacteria are strongly seasonal, but few attempts have been made to concurrently assess them across trophic levels. Here, we estimated the temperature sensitivities (using activation energies, E) of autotrophic and heterotrophic microbial plankton net growth rates over an annual cycle in NE Atlantic coastal waters. Phytoplankton grew in winter and late autumn (0.41 ± 0.16 SE d ) and decayed in the remaining months (-0.42 ± 0.10 d ). Heterotrophic microbes shared a similar seasonality, with positive net growth for bacteria (0.14-1.48 d ), while nanoflagellates had higher values (> 0.4 d ) in winter and spring relative to the rest of the year (-0.46 to 0.29 d ). Net growth rates activation energies showed similar dynamics in the three groups (-1.07 to 1.51 eV), characterized by maxima in winter, minima in summer and resumed increases in autumn. Microbial plankton E values were significantly correlated with nitrate concentrations as a proxy for nutrient availability. Nutrient-sufficiency (i.e., > 1 μmol l nitrate) resulted in significantly higher activation energies of phytoplankton and heterotrophic nanoflagellates relative to nutrient-limited conditions. We suggest that only within spatio-temporal windows of both moderate bottom-up and top-down controls will temperature have a major enhancing effect on microbial growth.

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

“…With regard to LNA cells, their negative specific growth rates in Mangrove and Seagrass became more negative with warming yielding equivalent E values of ca. −1 eV (see a more detailed discussion in the study by Morán et al ., ). Similar to the previous consideration, Dead cells cannot really have an activation energy, but we compared their apparent E values in order to assess their dynamics in response to temperature.…”

“…S5A). The same response has been recently reported for temperate phytoplankton under nutrient limitation (Morán et al ., ), suggesting that warming would exacerbate any metabolic and ecological processes resulting in either growth or decay of the various bacterial groups initially present.…”

“…Experimental incubations were performed at three different temperatures ( in situ plus 3°C below and above the ambient value in order to encompass 6°C without causing strong disturbance) aimed at comprehensively assessing the response of planktonic heterotrophic bacteria specific growth rates and carrying capacities at the individual level to allochthonous DOM and warming. The experimental response to temperature was described by the activation energies ( E ) of the metabolic theory of ecology (MTE) central equation (Brown et al ., ), as in previous work (Huete‐Stauffer et al ., ; Lønborg et al ., ; Morán et al ., ). Our hypotheses were (i) that heterotrophic bacteria growth would be enhanced by temperature in DOM‐rich conditions and (ii) that the contribution of the different physiological groups would change coherently with temperature and DOM.…”

Warming the phycosphere: Differential effect of temperature on the use of diatom‐derived carbon by two copiotrophic bacterial taxa

“…In the short‐term incubations carried out in this study, we found that experimental warming noticeably increased the abundance of microphytoplankton‐associated bacteria, while the effect on the free‐living community was less pronounced. Such larger effect of associated bacteria may be explained by at least two mechanisms: (i) increased chemotaxis ability to newly fixed DOC by the microphytoplankton‐associated bacteria (Smriga et al ., 2016), which would also promote a faster response to warming as the temperature sensitivity of bacteria is strongly related to the availability of resources (López‐Urrutia and Morán, 2007; Berggren et al ., 2010; Morán et al ., 2018), and/or (ii) a higher exudation of organic compounds by diatoms at higher temperatures, including transparent exopolymers particle (Claquin et al ., 2008; Wohlers et al ., 2009; Seebah et al ., 2014), which would facilitate bacterial aggregation (Mari and Kiørboe, 1996; Gardes et al ., 2011). In any case, we found that the impact of experimental warming was distinct for the entire associated bacterial community in comparison to the two taxa analysed and that it also exerted a noticeable larger effect on Flavobacteria than on Rhodobacteraceae, indicating a differential response of both taxonomic groups in terms of abundance, as previously observed in free‐living communities (von Scheibner et al ., 2014; Arandia‐Gorostidi et al ., 2017a).…”

Temperature and phosphorus interacts in controlling the picoplankton carbon flux in the Adriatic Sea: an experimental versus field study

“…However, in the case of BAC, the increase in temperature in May (from 21°C to 24°C) and July (from 23.6°C to 26.6°C) caused an increase in the growth rate only in the +P condition, which is supported by the study of Morán et al . () who found that the rise in temperature stimulates growth only in conditions of sufficient nutrients. This is particularly pronounced at temperatures above the optimal when bacterial growth slows down or stops.…”