Elevated temperature increases carbon and nitrogen fluxes between phytoplankton and heterotrophic bacteria through physical attachment

Abstract

Quantifying the contribution of marine microorganisms to carbon and nitrogen cycles and their response to predicted ocean warming is one of the main challenges of microbial oceanography. Here we present a single-cell NanoSIMS isotope analysis to quantify C and N uptake by free-living and attached phytoplankton and heterotrophic bacteria, and their response to short-term experimental warming of 4°C. Elevated temperature increased total C fixation by over 50%, a small but significant fraction of which was transferred to heterotrophs within 12 h. Cell-to-cell attachment doubled the secondary C uptake by heterotrophic bacteria and increased secondary N incorporation by autotrophs by 68%. Warming also increased the abundance of phytoplankton with attached heterotrophs by 80%, and promoted C transfer from phytoplankton to bacteria by 17% and N transfer from bacteria to phytoplankton by 50%. Our results indicate that phytoplankton-bacteria attachment provides an ecological advantage for nutrient incorporation, suggesting a mutualistic relationship that appears to be enhanced by temperature increases.

Attachment between heterotrophic bacteria and microalgae influences symbiotic microscale interactions

“…In general, attached bacteria assimilated more algal‐derived 13 C material than unattached bacteria, as shown previously in the coastal ocean (Arandia‐Gorostidi et al ., ). This could be explained by attached cells exhibiting higher bacterial growth efficiencies (BGEs) through incorporation and retention of more C in biomass compared to unattached cells using C for energy production.…”

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

“…In terms of cell‐specific uptake activity, the higher 13 C incorporation of microphytoplankton‐associated bacteria with increasing temperatures agrees with a previous study (Arandia‐Gorostidi et al ., 2017b), where only total bacterial communities were analysed, disregarding potential differences based on taxonomic affiliation. Here, we found a similar response in 13 C assimilation rates for the two taxa targeted, Flavobacteria and Rhodobacteraceae, indicating a comparable ability to incorporate algal‐derived DOC per cell volume, in contrast to the differences in absolute cell abundance found for both groups.…”

“…Examples of exceptionally high anaplerotic C assimilation have been demonstrated for some gammaproteobacterial taxa under starvation conditions (Alonso‐Sáez et al ., 2010), but it is unlikely that microphytoplankton‐associated bacteria experience carbon starvation. Furthermore, the C uptake rates observed in this work are of the same order of magnitude of those reported by earlier studies analysing algal‐derived DOC incorporation by heterotrophic bacteria (Adam et al ., 2016; Arandia‐Gorostidi et al ., 2017b). The fact that bacterial abundance was consistently higher in the presence of microphytoplankton (as compared to microphytoplankton‐free controls), also supports the view that most of the 13 C assimilation originated from algal‐derived DOC.…”

“…Trophic interactions between bacteria and microphytoplankton are influenced by the composition of bacterial communities (Pinhassi et al ., 2004; Grossart et al ., 2005; Klindworth et al ., 2014), as distinct taxonomic groups have different roles in the uptake of algal‐derived DOC (Teeling et al ., 2012). Some environmental parameters such as temperature may also have a key impact on these interactions, by promoting the C fluxes between both bacterial and phytoplankton communities (Arandia‐Gorostidi et al ., 2017b).…”

“…It has been proposed that bacteria associated with microphytoplankton may have stronger physical and metabolic interactions with microphytoplankton cells than their free‐living counterparts (Rooney‐Varga et al ., 2005; Grossart et al ., 2007), because the uptake of an important fraction of the microphytoplankton exudates takes place in this limited area where bacteria have fast access to recently fixed C (Smriga et al ., 2016). A previous study has indicated that increasing temperatures may have a higher impact on the C uptake by bacteria associated to phytoplankton than by their free‐living counterparts (Arandia‐Gorostidi et al ., 2017b). However, the temperature response of different bacterial taxa to the uptake of DOC is largely unknown, mostly due to the difficulties in coupling taxonomic identification and cell‐specific substrate uptakes in small‐scale environments such as the phycosphere.…”