Spatiotemporal dynamics of different CO2 fixation strategies used by prokaryotes in a dimictic lake

Albin Alfreider,Barbara Tartarotti

doi:10.1038/s41598-019-51584-0

Abstract

The Calvin-Benson-Bassham (CBB) cycle and the 3-hydroxypropionate/4-hydroxybutyrate (HP/HB) cycle are two inorganic carbon assimilation pathways widely used by prokaryotic autotrophs in lakes. We investigated the effect of mixing periods and stable water stratification patterns on the trajectories of both CO2 fixation strategies in a dimictic lake (Piburger See), because information on the spatiotemporal dynamics of prokaryotes using these pathways in freshwater ecosystems is far from complete. Based on a quantitative approach (droplet digital PCR) of genes coding for key enzymes in different CO2 assimilation pathways, nine depths covering the entire water column were investigated on a monthly basis for one year. Our data show that the abundance of photoautotrophs and obligate chemolithoautotrophs preferentially using form IA RubisCO was determined by seasonal variations. Highest numbers were observed in summer, while a strong decline of prokrayotes using RubisCO form IA was measured between December and May, the period where the lake was mostly covered by ice. The spatiotemporal distribution patterns of genes coding for RubisCO form IC genes, an enzyme usually used by facultative autotrophs for CO2 assimilation, were less pronounced. Bacteria harboring RubisCO form II were dominating the oxygen limited hypolimnion, while nitrifying Thaumarchaeota using the HP/HB cycle were of minor importance in the lake. Our data reveal that the seasonal heterogeneity, which is determined by the dimictic thermal regime of the lake, results in pronounced spatiotemporal changes of different CO2 assimilation pathways with depth-dependent environmental parameters as key factors for their distribution.

Highlights

The Calvin-Benson-Bassham (CBB) cycle and the 3-hydroxypropionate/4-hydroxybutyrate (HP/ HB) cycle are two inorganic carbon assimilation pathways widely used by prokaryotic autotrophs in lakes
Chlorophyll a (Chl a) levels peaked at the sampling date in April in the epilimnion (Fig. 1e), most probably caused by an algal spring bloom that occurs regularly in Piburger See at this time of the year[27,28,29]
Cyanobacteria and obligate chemolithoautotrophs using form IA RubisCO are generally highly specialized in their physiology and these organisms developed strong adaptation to narrow temporal ecological niches related to seasonal changes in the lake

Summary

Introduction

The Calvin-Benson-Bassham (CBB) cycle and the 3-hydroxypropionate/4-hydroxybutyrate (HP/ HB) cycle are two inorganic carbon assimilation pathways widely used by prokaryotic autotrophs in lakes. A previous investigation in seasonally stratified lake, based on a single sampling event during summer stratification, revealed a high diversity of sequences coding for three forms of RubisCO in the CBB cycle[6]. We were especially interested to follow the spatiotemporal variations of genes coding for different forms of RubisCO and to examine if the occurrence of these forms is related to seasonal changes of environmental variables. Another specific objective was to evaluate if the lack of autotrophic Thaumarchaeota during summer[6] occurs under ice during winter, when environmental conditions for chemoautotrophic growth are more favourable. Functional genes were correlated with limnological observations and environmental parameters in order to identify which physical and chemical drivers and processes are most influential for their quantitative occurrence

Methods

Results

Conclusion