Abstract
Zodletone spring is a sulfide-rich spring in southwestern Oklahoma characterized by shallow, microoxic, light-exposed spring water overlaying anoxic sediments. Previously, culture-independent 16S rRNA gene based diversity surveys have revealed that Zodletone spring source sediments harbor a highly diverse microbial community, with multiple lineages putatively involved in various sulfur-cycling processes. Here, we conducted a metatranscriptomic survey of microbial populations in Zodletone spring source sediments to characterize the relative prevalence and importance of putative phototrophic, chemolithotrophic, and heterotrophic microorganisms in the sulfur cycle, the identity of lineages actively involved in various sulfur cycling processes, and the interaction between sulfur cycling and other geochemical processes at the spring source. Sediment samples at the spring’s source were taken at three different times within a 24-h period for geochemical analyses and RNA sequencing. In depth mining of datasets for sulfur cycling transcripts revealed major sulfur cycling pathways and taxa involved, including an unexpected potential role of Actinobacteria in sulfide oxidation and thiosulfate transformation. Surprisingly, transcripts coding for the cyanobacterial Photosystem II D1 protein, methane monooxygenase, and terminal cytochrome oxidases were encountered, indicating that genes for oxygen production and aerobic modes of metabolism are actively being transcribed, despite below-detectable levels (<1 µM) of oxygen in source sediment. Results highlight transcripts involved in sulfur, methane, and oxygen cycles, propose that oxygenic photosynthesis could support aerobic methane and sulfide oxidation in anoxic sediments exposed to sunlight, and provide a viewpoint of microbial metabolic lifestyles under conditions similar to those seen during late Archaean and Proterozoic eons.
Highlights
The combination of molecular techniques and high-throughput sequencing in microbial ecology has revolutionized the ability to probe questions regarding microbial community structure and function (Handelsman, 2004)
Geochemistry of Zodletone spring water Sulfide measurements from source water samples at the time of sampling (Nov, 2009) and again in Aug, 2014, indicated a progressive decrease in sulfide values during the day, followed by increase in sulfide levels overnight (Fig. 1). These results confirm previous findings from two previous studies that utilized either direct geochemical measurements at the spring source or laboratory incubations of spring source sediments, and demonstrated that sulfate production from sulfide is primarily a light-dependent process, whereas sulfate reduction/sulfidogenesis occurs predominately nocturnally/in dark incubations (Elshahed et al, 2003; Senko et al, 2004). The results of these studies conducted over more than a decade, along with the documentation of a similar pattern in this study (Fig. 1), demonstrate that the observed sulfur cycling dynamics in Zodletone spring source water is an ecologically relevant and temporally stable process, with sulfur oxidative processes occurring during the day and reductive processes increasing at night
The study provides insight into a complex sulfur cycle that includes the possible involvement of Actinobacteria in sulfur transformations and identifies several interesting features not previously documented in the anoxic sediments of this high-sulfide sunlight-exposed aquatic spring, including a full methane cycle, with activity of Type I methanotrophs at night and the likelihood of O2 production and utilization through oxygenic photosynthesis and aerobic metabolism, respectively
Summary
The combination of molecular techniques and high-throughput sequencing in microbial ecology has revolutionized the ability to probe questions regarding microbial community structure and function (Handelsman, 2004). Metagenomic and metatranscriptomic approaches have provided valuable insights into the roles of uncultivated lineages within a microbial community (Pelletier et al, 2008; Liu et al, 2012; Kozubal et al, 2013; Sheik, Jain & Dick, 2014) as well as in delineating the relative importance and contributions of various microbial taxa to observed geochemical processes occurring in habitats characterized by complex biodiversity, such as soil (Urich et al, 2008; Shrestha et al, 2009), surface and deep ocean water (Poretsky et al, 2005; Frias-Lopez et al, 2008; Poretsky et al, 2009; Baker et al, 2013), deep ocean hydrothermal vent systems (Xie et al, 2010; Lesniewski et al, 2012), and hot springs (Liu et al, 2011; Burow et al, 2013). The water overlying the sediments has low O2 concentrations (2–4 μM) (Buhring et al, 2011), high levels of methane from the subsurface, and high concentrations of sulfur in various forms (Donovan, Younger & Ditzell, 1988)
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