Testing the metabolic theory of ecology with marine bacteria: different temperature sensitivity of major phylogenetic groups during the spring phytoplankton bloom

Abstract

Although temperature is a key driver of bacterioplankton metabolism, the effect of ocean warming on different bacterial phylogenetic groups remains unclear. Here, we conducted monthly short-term incubations with natural coastal bacterial communities over an annual cycle to test the effect of experimental temperature on the growth rates and carrying capacities of four phylogenetic groups: SAR11, Rhodobacteraceae, Gammaproteobacteria and Bacteroidetes. SAR11 was the most abundant group year-round as analysed by CARD-FISH, with maximum abundances in summer, while the other taxa peaked in spring. All groups, including SAR11, showed high temperature-sensitivity of growth rates and/or carrying capacities in spring, under phytoplankton bloom or post-bloom conditions. In that season, Rhodobacteraceae showed the strongest temperature response in growth rates, estimated here as activation energy (E, 1.43 eV), suggesting an advantage to outcompete other groups under warmer conditions. In summer E values were in general lower than 0.65 eV, the value predicted by the Metabolic Theory of Ecology (MTE). Contrary to MTE predictions, carrying capacity tended to increase with warming for all bacterial groups. Our analysis confirms that resource availability is key when addressing the temperature response of heterotrophic bacterioplankton. We further show that even under nutrient-sufficient conditions, warming differentially affected distinct bacterioplankton taxa.

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

“…Thus, to test the temperature sensitivity of Flavobacteria and Rhodobacteraceae over a realistic range in this scenario, we used 3°C above ambient temperature as the warm treatment. Additionally, we also included a colder treatment (3°C below ambient temperature) in order to have a range as broad as possible without putting the communities into thermal stress (Huete‐Stauffer et al ., 2016; Arandia‐Gorostidi et al ., 2017a). Since short‐incubation experiments do not consider potential long‐term effects such as bacterial acclimation in response to slow environmental change, caution should be taken when interpreting results obtained from this type of experiments.…”

“…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). Adaptations to detect and exploit DOC hotspots have been well described in both Rhodobacteraceae and Flavobacteria (Miller et al ., 2004; Buchan et al ., 2005; Fernández‐Gómez et al ., 2013).…”

“…Yet, the observed higher response of Flavobacteria to warming suggests that this group may be better adapted to use the newly released DOC within the phycosphere. Interestingly, in a previous study at the same site, we observed that the response to increasing temperature of free‐living Rhodobacteraceae was stronger than that of Flavobacteria (Arandia‐Gorostidi et al ., 2017a), suggesting that the response to warming may differ in each fraction. However, since in the latter study the effect of warming was exclusively tested on the growth rates (not on abundances) of the free‐living community, the results of both studies are not fully comparable.…”

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

“…Temperature appears to play a major role at low temperatures, when substrates are in excess due to phytoplankton blooming in spring and autumn after water-column mixing brings new nutrients into the surface layers (Ducklow et al, 2002), whereas nutrient-limitation in summer stratified conditions would render temperature unimportant in promoting microbial growth (Calvo-Díaz et al, 2014;Morán et al, 2010). This hypothesis has been recently confirmed experimentally in temperate coastal waters (Huete-Stauffer et al, 2015;Arandia-Gorostidi et al, 2017). On a large geographical scale, temperature regulation of heterotrophic bacteria and archaea decreased toward the Equator .…”

“…Monthly temperature manipulation experiments in coastal NE Atlantic waters showed a marked seasonality in the activation energies of heterotrophic bacterioplankton specific growth rates (Huete-Stauffer et al, 2015;Arandia-Gorostidi et al, 2017). Values close to the predicted 0.65 eV were only reached in late winter and spring, coincident with the presence of seasonally recurring phytoplankton blooms in the region (Bode et al, 2011), suggesting that resource availability was a pre-requisite for temperature to drive bacterial growth.…”