Abstract
Because the nature of the main resource that limits bacterioplankton (e.g. organic carbon [C] or phosphorus [P]) has biogeochemical implications concerning organic C accumulation in freshwater ecosystems, empirical knowledge is needed concerning how bacteria respond to these two resources, available alone or together. We performed field experiments of resource manipulation (2×2 factorial design, with the addition of C, P, or both combined) in two Mediterranean freshwater ecosystems with contrasting trophic states (oligotrophy vs. eutrophy) and trophic natures (autotrophy vs. heterotrophy, measured as gross primary production:respiration ratio). Overall, the two resources synergistically co-limited bacterioplankton, i.e. the magnitude of the response of bacterial production and abundance to the two resources combined was higher than the additive response in both ecosystems. However, bacteria also responded positively to single P and C additions in the eutrophic ecosystem, but not to single C in the oligotrophic one, consistent with the value of the ratio between bacterial C demand and algal C supply. Accordingly, the trophic nature rather than the trophic state of the ecosystems proves to be a key feature determining the expected types of resource co-limitation of bacteria, as summarized in a proposed theoretical framework. The actual types of co-limitation shifted over time and partially deviated (a lesser degree of synergism) from the theoretical expectations, particularly in the eutrophic ecosystem. These deviations may be explained by extrinsic ecological forces to physiological limitations of bacteria, such as predation, whose role in our experiments is supported by the relationship between the dynamics of bacteria and bacterivores tested by SEMs (structural equation models). Our study, in line with the increasingly recognized role of freshwater ecosystems in the global C cycle, suggests that further attention should be focussed on the biotic interactions that modulate resource co-limitation of bacteria.
Highlights
In aquatic ecosystems, bacterioplankton is regulated by different factors [1], including: abiotic such as temperature [2,3,4] or inorganic and organic nutrient sources [5,6]; and biotic, such as predation [7,8,9]
Bacteria are presumed to be P limited in oligotrophic lakes [19,20] and/or in those with high dissolved organic carbon (DOC):P ratios [21], despite that bacteria have a greater affinity for P than do phytoplankton in P-poor aquatic ecosystems [18,22,23]
Water temperature reached only 14uC in La Caldera, with a homogeneous vertical profile to the maximum depth (10 m). Chemical variables, such as DOC, TP, and TN showed values between 5- and 9-fold higher in Cubillas than in La Caldera, representing the contrasting trophic states of the two ecosystems. This difference was further indicated by water transparency (Secchi disk depth was 18-fold higher in La Caldera) and the biotic variables, which showed higher values in Cubillas than in La Caldera (Chl a, 3.6-fold; algal biomass, 44-fold; Bacterial abundance (BA), 10.3-fold; bacterial production (BP), 16.1-fold; R [,45 mm fraction], 3.8-fold; bacterial respiration (BR) [,1.2 mm fraction], 8.9-fold; Table 1)
Summary
Bacterioplankton is regulated by different factors [1], including: abiotic such as temperature [2,3,4] or inorganic and organic nutrient sources [5,6]; and biotic, such as predation [7,8,9]. Heterotrophic bacteria remineralize nutrients [1,12,13] via general or specialized biogeochemical pathways and, in turn, transfer them to high trophic levels through the microbial loop [14,15]. In this regard, bacteria convert dissolved organic carbon (DOC) to biomass throughout bacterial production (BP) and/or oxidize it to CO2 through bacterial respiration (BR) [16]. If bacteria are limited by inorganic nutrients, e.g. P, the labile share of the C pool accumulates in the ecosystem. A prevalence of mineral-nutrient and organic carbon co-limitation in aquatic microbial communities, deduced from stronger responses to combined resources than to single-nutrient additions [13,26]
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