Changes in the phytoplankton-bacteria coupling triggered by joint action of UVR, nutrients, and warming in Mediterranean high-mountain lakes

Abstract

From an extensive study, we determined that heterotrophic bacterial production (HBP) variance in Sierra Nevada (Spain) lakes was explained mainly by excretion of organic carbon by algae (EOC), underlining a bacterial dependence on algal carbon. Subsequently, we studied how the interaction among global change factors such as ultraviolet radiation (UVR), nutrient inputs, and increased temperature affected this phytoplankton-bacteria coupling through in situ factorial experiments in two model high-mountain lakes, La Caldera, and Las Yeguas. Bacterioplankton were more sensitive than phytoplankton because the joint action of increased temperature and nutrient-addition unmasked an inhibitory UVR effect on HBP while reducing the inhibitory UVR effect on primary production (PP) (in La Caldera) or augmenting the net PP values (in Las Yeguas). The interaction among the three factors had a different effect on phytoplankton-bacteria coupling depending on the lake. Thus, in the colder lake (La Caldera), EOC was not adequate to meet the bacterial carbon demand (BCD), leading to a mismatch in phytoplankton-bacteria coupling. Contrarily, in the warmer lake (Las Yeguas), the phytoplankton-bacteria coupling was accentuated by the interaction among the three factors, with EOC exceeding BCD. These contrasting responses of phytoplankton-bacteria coupling may affect the microbial loop development, becoming reinforced in warmer and less UVR-transparent highmountain lakes, but weakened in colder and more UVR-transparent high-mountain lakes, with implications in the C-flux of these sentinel ecosystems in a scenario of global change.

Uncoupled phytoplankton-bacterioplankton relationship by multiple drivers interacting at different temporal scales in a high-mountain Mediterranean lake

“…Furthermore, the increased P availability may prompt a more efficient utilization of dissolved organic carbon (DOC) by bacterioplankton, either from photolysis 52 , from algal EOC or viral lysis 47 . Although our experimental approach was not designed to evaluate dissolved organic-matter utilization by bacteria, the lack of a significant relationship between EOC and HBP in this experiment suggests that bacterial community under UVR and P addition was not primarily controlled by the availability of fresh-released photosynthetic carbon, but rather by other biotic controls, such as top-down control exerted mainly by lithic viral cycles 46,53 that could break the bacterial dependence on EOC, usually evidenced in La Caldera 39,54 . In this line, previous findings also evidenced how the influence of other biotic components could also break phytoplankton-bacterioplankton coupling (bacterial dependence on phytoplanktonic carbon), such as the control on bacteria through P recycled by high zooplankton abundance 55 .…”

“…Few experiments have focused on the interactive effects of UVR, nutrients, and temperature on phytoplankton and/or bacterioplankton [37][38][39] , and only one report has described the effects of these three factors on phytoplankton-bacterioplankton relationship in Mediterranean high-mountain lakes 39 . Recently, in Sierra Nevada high-mountain lakes (southern Spain) has been found a shift in phytoplankton-bacterioplankton relationship from a dual commensalistic-bacterivory control exerted by phytoplankton 40 to a predominant commensalism under conditions of higher temperature and nutrient inputs after a decade of global change 22 .…”

“…Recently, in Sierra Nevada high-mountain lakes (southern Spain) has been found a shift in phytoplankton-bacterioplankton relationship from a dual commensalistic-bacterivory control exerted by phytoplankton 40 to a predominant commensalism under conditions of higher temperature and nutrient inputs after a decade of global change 22 . Moreover, the strength of phytoplankton-bacterioplankton commensalistic relationship is quickly modulated by the interactive effect among UVR, nutrient inputs and warming by mismatching phytoplankton-bacteria coupling 39 .…”

Contrasting effect of Saharan dust and UVR on autotrophic picoplankton in nearshore versus offshore waters of Mediterranean Sea

“…Thus, the increasing stimulatory UVR effect on NPQ under dust addition over the experiment makes a higher degree of stress evident. This unmasking of a harmful UVR effect on PP and productivity after nutrient enrichment has been widely reported in oligotrophic freshwater [ Carrillo et al ., ; Korbee et al ., ; Durán et al ., ] as well as in coastal ecosystems [ Carrillo et al ., ]. Furthermore, this negative synergistic effect on APP could be related to higher rates of DNA synthesis due to stimulated growth induced by the addition of dust rich in limiting nutrients.…”

Warming and nutrient enrichment in combination increase stochasticity and beta diversity of bacterioplankton assemblages across freshwater mesocosms

“…Bacterioplankton, an integral component of the planktonic food webs in shallow lake ecosystems, perform important tasks in regenerating nutrients and decomposing organic matter (Hall and Cotner, 2007;Ruiz-González et al, 2015). Currently, studies of warming effects on the lacustrine bacterioplankton community have mainly focused on bacterioplankton growth traits, such as cell densities (Baulch et al, 2005), abundance (Christoffersen et al, 2006;Markensten et al, 2010), biomass (Hall et al, 2009;Shurin et al, 2012;Özen et al, 2013), metabolism (Hall and Cotner, 2007;Hall et al, 2008) and production (Durán et al, 2016). Most of these studies suggest that warming, when interacting with eutrophication, enhances the growth of lacustrine bacterioplankton (Christoffersen et al, 2006;Shurin et al, 2012;Özen et al, 2013).…”