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1. Groundwater shapes sediment biogeochemistry and microbial diversity in a submerged Great Lake sinkhole

   https://doi.org/10.1111/gbi.12215  

   Kinsman‐Costello, L. E. ; Sheik, C. S. ; Sheldon, N. D. ; Allen Burton, G. ; Costello, D. M. ; Marcus, D. ; Uyl, P. A. Den ; Dick, G. J. ( September 2016 , Geobiology)

   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 (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 byPhormidiumandPlanktothrixthat 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 16SrRNAgene 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 theMISwere distinctly different from those in typicalLHsediments 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 toMISmicrobial community composition, whileLHcommunities 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.

    

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2. Metabolic Capacity of the Antarctic Cyanobacterium Phormidium pseudopriestleyi That Sustains Oxygenic Photosynthesis in the Presence of Hydrogen Sulfide

   https://doi.org/10.3390/genes12030426  

   Lumian, Jessica E. ; Jungblut, Anne D. ; Dillion, Megan L. ; Hawes, Ian ; Doran, Peter T. ; Mackey, Tyler J. ; Dick, Gregory J. ; Grettenberger, Christen L. ; Sumner, Dawn Y. ( March 2021 , Genes)

   null (Ed.)

   Sulfide inhibits oxygenic photosynthesis by blocking electron transfer between H2O and the oxygen-evolving complex in the D1 protein of Photosystem II. The ability of cyanobacteria to counter this effect has implications for understanding the productivity of benthic microbial mats in sulfidic environments throughout Earth history. In Lake Fryxell, Antarctica, the benthic, filamentous cyanobacterium Phormidium pseudopriestleyi creates a 1–2 mm thick layer of 50 µmol L−1 O2 in otherwise sulfidic water, demonstrating that it sustains oxygenic photosynthesis in the presence of sulfide. A metagenome-assembled genome of P. pseudopriestleyi indicates a genetic capacity for oxygenic photosynthesis, including multiple copies of psbA (encoding the D1 protein of Photosystem II), and anoxygenic photosynthesis with a copy of sqr (encoding the sulfide quinone reductase protein that oxidizes sulfide). The genomic content of P. pseudopriestleyi is consistent with sulfide tolerance mechanisms including increasing psbA expression or directly oxidizing sulfide with sulfide quinone reductase. However, the ability of the organism to reduce Photosystem I via sulfide quinone reductase while Photosystem II is sulfide-inhibited, thereby performing anoxygenic photosynthesis in the presence of sulfide, has yet to be demonstrated. 

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3. Sedimentary pyrite sulfur isotope compositions preserve signatures of the surface microbial mat environment in sediments underlying low‐oxygen cyanobacterial mats

   https://doi.org/10.1111/gbi.12466  

   Gomes, Maya L. ; Klatt, Judith M. ; Dick, Gregory J. ; Grim, Sharon L. ; Rico, Kathryn I. ; Medina, Matthew ; Ziebis, Wiebke ; Kinsman‐Costello, Lauren ; Sheldon, Nathan D. ; Fike, David A. ( July 2021 , Geobiology)

   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.

    

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4. Seasonal shifts in community composition and proteome expression in a sulphur‐cycling cyanobacterial mat

   https://doi.org/10.1111/1462-2920.16480  

   Grim, Sharon L. ; Stuart, Dack G. ; Aron, Phoebe ; Levin, Naomi E. ; Kinsman‐Costello, Lauren ; Waldbauer, Jacob R. ; Dick, Gregory J. ( August 2023 , Environmental Microbiology)

   Seasonal changes in light and physicochemical conditions have strong impacts on cyanobacteria, but how they affect community structure, metabolism, and biogeochemistry of cyanobacterial mats remains unclear. Light may be particularly influential for cyanobacterial mats exposed to sulphide by altering the balance of oxygenic photosynthesis and sulphide‐driven anoxygenic photosynthesis. We studied temporal shifts in irradiance, water chemistry, and community structure and function of microbial mats in the Middle Island Sinkhole (MIS), where anoxic and sulphate‐rich groundwater provides habitat for cyanobacteria that conduct both oxygenic and anoxygenic photosynthesis. Seasonal changes in light and groundwater chemistry were accompanied by shifts in bacterial community composition, with a succession of dominant cyanobacteria fromPhormidiumtoPlanktothrix, and an increase in diatoms, sulphur‐oxidizing bacteria, and sulphate‐reducing bacteria from summer to autumn. Differential abundance of cyanobacterial light‐harvesting proteins likely reflects a physiological response of cyanobacteria to light level.Beggiatoasulphur oxidation proteins were more abundant in autumn. Correlated abundances of taxa through time suggest interactions between sulphur oxidizers and sulphate reducers, sulphate reducers and heterotrophs, and cyanobacteria and heterotrophs. These results support the conclusion that seasonal change, including light availability, has a strong influence on community composition and biogeochemical cycling of sulphur and O₂in cyanobacterial mats.

    

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5. Metatranscriptomic analysis of a high-sulfide aquatic spring reveals insights into sulfur cycling and unexpected aerobic metabolism

   https://doi.org/10.7717/peerj.1259  

   Spain, Anne M. ; Elshahed, Mostafa S. ; Najar, Fares Z. ; Krumholz, Lee R. ( September 2015 , PeerJ)

   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.

    

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