For a large part of earth's history, cyanobacterial mats thrived in low‐oxygen conditions, yet our understanding of their ecological functioning is limited. Extant cyanobacterial mats provide windows into the putative functioning of ancient ecosystems, and they continue to mediate biogeochemical transformations and nutrient transport across the sediment–water interface in modern ecosystems. The structure and function of benthic mats are shaped by biogeochemical processes in underlying sediments. A modern cyanobacterial mat system in a submerged sinkhole of Lake Huron (
Biogeochemical sulfur cycling in sulfidic karst systems is largely driven by abiotic and biological sulfide oxidation, but the fate of elemental sulfur (S0) that accumulates in these systems is not well understood. The Frasassi Cave system (Italy) is intersected by a sulfidic aquifer that mixes with small quantities of oxygen‐rich meteoric water, creating Proterozoic‐like conditions and supporting a prolific ecosystem driven by sulfur‐based chemolithoautotrophy. To better understand the cycling of S0in this environment, we examined the geochemistry and microbiology of sediments underlying widespread sulfide‐oxidizing mats dominated by
- NSF-PAR ID:
- 10469374
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Geobiology
- Volume:
- 21
- Issue:
- 6
- ISSN:
- 1472-4677
- Format(s):
- Medium: X Size: p. 791-803
- Size(s):
- ["p. 791-803"]
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Abstract LH ) provides a unique opportunity to explore such sediment–mat interactions. In the Middle Island Sinkhole (MIS ), seeping groundwater establishes a low‐oxygen, sulfidic environment in which a microbial mat dominated byPhormidium andPlanktothrix that is capable of both anoxygenic and oxygenic photosynthesis, as well as chemosynthesis, thrives. We explored the coupled microbial community composition and biogeochemical functioning of organic‐rich, sulfidic sediments underlying the surface mat. Microbial communities were diverse and vertically stratified to 12 cm sediment depth. In contrast to previous studies, which used low‐throughput or shotgun metagenomic approaches, our high‐throughput 16SrRNA gene sequencing approach revealed extensive diversity. This diversity was present within microbial groups, including putative sulfate‐reducing taxa ofDeltaproteobacteria , some of which exhibited differential abundance patterns in the mats and with depth in the underlying sediments. The biological and geochemical conditions in theMIS were distinctly different from those in typicalLH sediments of comparable depth. We found evidence for active cycling of sulfur, methane, and nutrients leading to high concentrations of sulfide, ammonium, and phosphorus in sediments underlying cyanobacterial mats. Indicators of nutrient availability were significantly related toMIS microbial community composition, whileLH communities were also shaped by indicators of subsurface groundwater influence. These results show that interactions between the mats and sediments are crucial for sustaining this hot spot of biological diversity and biogeochemical cycling. -
more » « less
Abstract The sedimentary pyrite sulfur isotope (δ34S) record is an archive of ancient microbial sulfur cycling and environmental conditions. Interpretations of pyrite δ34S signatures in sediments deposited in microbial mat ecosystems are based on studies of modern microbial mat porewater sulfide δ34S geochemistry. Pyrite δ34S values often capture δ34S signatures of porewater sulfide at the location of pyrite formation. However, microbial mats are dynamic environments in which biogeochemical cycling shifts vertically on diurnal cycles. Therefore, there is a need to study how the location of pyrite formation impacts pyrite δ34S patterns in these dynamic systems. Here, we present diurnal porewater sulfide δ34S trends and δ34S values of pyrite and iron monosulfides from Middle Island Sinkhole, Lake Huron. The sediment–water interface of this sinkhole hosts a low‐oxygen cyanobacterial mat ecosystem, which serves as a useful location to explore preservation of sedimentary pyrite δ34S signatures in early Earth environments. Porewater sulfide δ34S values vary by up to ~25‰ throughout the day due to light‐driven changes in surface microbial community activity that propagate downwards, affecting porewater geochemistry as deep as 7.5 cm in the sediment. Progressive consumption of the sulfate reservoir drives δ34S variability, instead of variations in average cell‐specific sulfate reduction rates and/or sulfide oxidation at different depths in the sediment. The δ34S values of pyrite are similar to porewater sulfide δ34S values near the mat surface. We suggest that oxidative sulfur cycling and other microbial activity promote pyrite formation in and immediately adjacent to the microbial mat and that iron geochemistry limits further pyrite formation with depth in the sediment. These results imply that primary δ34S signatures of pyrite deposited in organic‐rich, iron‐poor microbial mat environments capture information about microbial sulfur cycling and environmental conditions at the mat surface and are only minimally affected by deeper sedimentary processes during early diagenesis.
-
Bernstein, Hans C. (Ed.)ABSTRACT Cyanobacterial mats profoundly influenced Earth’s biological and geochemical evolution and still play important ecological roles in the modern world. However, the biogeochemical functioning of cyanobacterial mats under persistent low-O 2 conditions, which dominated their evolutionary history, is not well understood. To investigate how different metabolic and biogeochemical functions are partitioned among community members, we conducted metagenomics and metatranscriptomics on cyanobacterial mats in the low-O 2 , sulfidic Middle Island sinkhole (MIS) in Lake Huron. Metagenomic assembly and binning yielded 144 draft metagenome assembled genomes, including 61 of medium quality or better, and the dominant cyanobacteria and numerous Proteobacteria involved in sulfur cycling. Strains of a Phormidium autumnale -like cyanobacterium dominated the metagenome and metatranscriptome. Transcripts for the photosynthetic reaction core genes psaA and psbA were abundant in both day and night. Multiple types of psbA genes were expressed from each cyanobacterium, and the dominant psbA transcripts were from an atypical microaerobic type of D1 protein from Phormidium . Further, cyanobacterial transcripts for photosystem I genes were more abundant than those for photosystem II, and two types of Phormidium sulfide quinone reductase were recovered, consistent with anoxygenic photosynthesis via photosystem I in the presence of sulfide. Transcripts indicate active sulfur oxidation and reduction within the cyanobacterial mat, predominately by Gammaproteobacteria and Deltaproteobacteria , respectively. Overall, these genomic and transcriptomic results link specific microbial groups to metabolic processes that underpin primary production and biogeochemical cycling in a low-O 2 cyanobacterial mat and suggest mechanisms for tightly coupled cycling of oxygen and sulfur compounds in the mat ecosystem. IMPORTANCE Cyanobacterial mats are dense communities of microorganisms that contain photosynthetic cyanobacteria along with a host of other bacterial species that play important yet still poorly understood roles in this ecosystem. Although such cyanobacterial mats were critical agents of Earth’s biological and chemical evolution through geological time, little is known about how they function under the low-oxygen conditions that characterized most of their natural history. Here, we performed sequencing of the DNA and RNA of modern cyanobacterial mat communities under low-oxygen and sulfur-rich conditions from the Middle Island sinkhole in Lake Huron. The results reveal the organisms and metabolic pathways that are responsible for both oxygen-producing and non-oxygen-producing photosynthesis as well as interconversions of sulfur that likely shape how much O 2 is produced in such ecosystems. These findings indicate tight metabolic reactions between community members that help to explain the limited the amount of O 2 produced in cyanobacterial mat ecosystems.more » « less
-
more » « less
Summary Chemotrophic microorganisms gain energy for cellular functions by catalyzing oxidation–reduction (redox) reactions that are out of equilibrium. Calculations of the Gibbs energy (
ΔG r ΔG r + 2H+ ⇌ 4S0+ 4H2O). We show that at elevated concentrations of sulfide and sulfate in acidic environments over a broad temperature range, this putative metabolism can be exergonic (ΔG r ⇌ + H2O) and to sulfite (H2S + 3 ⇌ 4+ 2H+), are only moderately exergonic or endergonic even at ideal geochemical conditions. Natural and impacted environments, including sulfidic karst systems, shallow‐sea hydrothermal vents, sites of acid mine drainage, and acid–sulfate crater lakes, may be ideal hunting grounds for finding microbial sulfur comproportionators. -
more » « less
Abstract Microbial sulfur cycling in marine sediments often occurs in environments characterized by transient chemical gradients that affect both the availability of nutrients and the activity of microbes. High turnover rates of intermediate valence sulfur compounds and the intermittent availability of oxygen in these systems greatly impact the activity of sulfur‐oxidizing micro‐organisms in particular. In this study, the thiosulfate‐oxidizing hydrothermal vent bacterium
Thiomicrospira thermophila strain EPR85 was grown in continuous culture at a range of dissolved oxygen concentrations (0.04–1.9 mM) and high pressure (5–10 MPa) in medium buffered at pH 8. Thiosulfate oxidation under these conditions produced tetrathionate, sulfate, and elemental sulfur, in contrast to previous closed‐system experiments at ambient pressure during which thiosulfate was quantitatively oxidized to sulfate. The maximum observed specific growth rate at 5 MPa pressure under unlimited O2was 0.25 hr−1. This is comparable to theμ max(0.28 hr−1) observed at low pH (<6) at ambient pressure whenT. thermophila produces the same mix of sulfur species. The half‐saturation constant for O2() estimated from this study was 0.2 mM (at a cell density of 105cells/ml) and was robust at all pressures tested (0.4–10 MPa), consistent with piezotolerant behavior of this strain. The cell‐specific was determined to be 1.5 pmol O2/cell. The concentrations of products formed were correlated with oxygen availability, with tetrathionate production in excess of sulfate production at all pressure conditions tested. This study provides evidence for transient sulfur storage during times when substrate concentration exceeds cell‐specific and subsequent consumption when oxygen dropped below that threshold. These results may be common among sulfur oxidizers in a variety of environments (e.g., deep marine sediments to photosynthetic microbial mats).
