Abstract
Seasonal wind-driven upwelling, high primary production in surface waters, and oxygen deficiency in subsurface waters characterize the coastal ecosystem of the subtropical eastern South Pacific (ESP), and shape the nature and dynamics of the microbial community structure and function. We investigated the diversity, abundance, and transcriptional levels of the gene encoding the large subunit form II of the RuBisCO enzyme (cbbM) in the pelagic microbial community at a continental-shelf site off central Chile over two years. We focused on cbbM genes affiliated with the sulfur-oxidizing -proteobacteria cluster, whose members are known to dominate in oxygen-deficient marine environments and are highly abundant in the study area. Phylogenetic analysis of cbbM sequences suggests the presence of a novel group of chemolithoautotrophs, closely related to the SUP05/ARCTIC96BD-19 clade. Through (RT)-qPCR, we studied the cbbM gene abundance and transcript dynamics over an annual cycle, finding a significantly higher number of cbbM copies per unit volume in months of active upwelling and at depths in which oxygen was scarce or absent. The same temporal pattern was observed at the transcriptional level. We also analyzed the relative expression of key genes for carbon, nitrogen and sulfur cycling in six metatranscriptomic datasets, for two characteristic periods within the annual cycle: the anoxic upwelling and the suboxic downwelling. Our results indicate that coastal waters of the subtropical ESP contain transcriptionally active populations of carbon fixing pelagic bacteria, whose dynamics is controlled, in large part, by fluctuations in oxygen levels. They also suggest that chemolithoautotrophic processes coupled to the sulfur and nitrogen cycles become increasingly important for the carbon economy of marine coastal waters as oxygen concentrations decline.
Highlights
The majority of primary production in the global ocean is carried out by cyanobacteria and photosynthetic eukaryotic algae in the upper ocean, using the Calvin-BensonBassham (CBB) cycle for inorganic carbon fixation
Studies on molecular taxonomy have indicated that sulfur-oxidizing γproteobacteria of the SUP05/ARCTIC96BD-19 clade dominate microbial communities present in oxygen-deficient marine pelagic systems (Stevens and Ulloa, 2008; Lavik et al, 2009; Walsh et al, 2009; Stewart et al, 2012; Wright et al, 2012; Glaubitz et al, 2013; Schunck et al, 2013)
We have assessed the diversity, abundance and transcriptional levels of the cbbM gene and other key genes involved in the sulfur and nitrogen cycles, cycles that have been proposed to be coupled by this group of sulfur-oxidizing γ-proteobacteria
Summary
The majority of primary production in the global ocean is carried out by cyanobacteria and photosynthetic eukaryotic algae in the upper ocean (the photic zone), using the Calvin-BensonBassham (CBB) cycle for inorganic carbon fixation. RuBisCO form I is found in most of chemoand photoautotrophic bacteria, cyanobacteria, eukaryotic plankton, algae and plants, it is adapted to aerobic conditions and its role in carbon fixation by planktonic photoautotrophs (expression levels, rates of fixation and diel cycle) has been studied extensively in different aquatic environments (Pichard et al, 1993; Xu and Tabita, 1996; Corredor et al, 2004; Tabita et al, 2007a). Form II presents a low specificity factor s, which is a measure of the ability of the enzyme to discriminate between CO2 and O2 at a given ratio This implies that form II is adapted to operate in low-O2 and high-CO2 concentration environments (Badger and Bek, 2007; Tabita et al, 2008), but studies on its expression levels and role in dark carbon fixation in natural communities are scarce
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