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1. Omics-Inferred Partitioning and Expression of Diverse Biogeochemical Functions in a Low-O 2 Cyanobacterial Mat Community

   https://doi.org/10.1128/mSystems.01042-21  

   Grim, Sharon L. ; Voorhies, Alexander A. ; Biddanda, Bopaiah A. ; Jain, Sunit ; Nold, Stephen C. ; Green, Russ ; Dick, Gregory J. ( December 2021 , mSystems)

   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. 

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2. 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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3. Associations between redox‐sensitive trace metals and microbial communities in a Proterozoic ocean analogue

   https://doi.org/10.1111/gbi.12388  

   Rico, Kathryn I. ; Sheldon, Nathan D. ; Kinsman‐Costello, Lauren E. ( March 2020 , Geobiology)

   Constraints on Precambrian ocean chemistry are dependent upon sediment geochemistry. However, diagenesis and metamorphism can destroy primary biosignatures, making it difficult to consider biology when interpreting geochemical data. Modern analogues for ancient ecosystems can be useful tools for identifying how sediment geochemistry records an active biosphere. The Middle Island Sinkhole (MIS) in Lake Huron is an analogue for shallow Proterozoic waters due to its low oxygen water chemistry and microbial communities that exhibit diverse metabolic functions at the sediment–water interface. This study uses sediment trace metal contents and microbial abundances in MIS sediments and an oxygenated Lake Huron control site (LH) to infer mechanisms for trace metal burial. The adsorption of trace metals to Mn‐oxyhydroxides is a critical burial pathway for metals in oxic LH sediments, but not for the MIS mat and sediments, consistent with conventional understanding of Mn cycling. Micronutrient trace metals (e.g., Zn) are associated with organic matter regardless of oxygen and sulfide availability. Although U and V are conventionally considered to be organically complexed in suboxic and anoxic conditions, U and organic covary in oxic LH sediments, and Mn‐oxyhydroxide cycling dominates V deposition in the anoxic MIS sediments. Significant correlations between Mo and organic matter across all redox regimes have major implications for our interpretations of Mo isotope systematics in the geologic record. Finally, while microbial groups vary between the sampling locales (e.g., the cyanobacteria in the MIS microbial mat are not present in LH sediments), LH and MIS ultimately have similar relationships between microbial assemblages and metal burial, making it difficult to link trace metal burial to microbial metabolisms. Together, these results indicate that bulk sediment trace metal composition does not capture microbiological processes; more robust trace metal geochemistry such as isotopes and speciation may be critical for understanding the intersections between microbiology and sediment geochemistry.

    

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4. Sulfur disproportionating microbial communities in a dynamic, microoxic‐sulfidic karst system

   https://doi.org/10.1111/gbi.12574  

   Aronson, Heidi S. ; Clark, Christian E. ; LaRowe, Douglas E. ; Amend, Jan P. ; Polerecky, Lubos ; Macalady, Jennifer L. ( September 2023 , Geobiology)

   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 byBeggiatoa. Sediment populations were dominated by uncultivated relatives of sulfur cycling chemolithoautotrophs related toSulfurovum,Halothiobacillus,Thiofaba,Thiovirga,Thiobacillus, andDesulfocapsa, as well as diverse uncultivated anaerobic heterotrophs affiliated withBacteroidota, Anaerolineaceae, Lentimicrobiaceae, and Prolixibacteraceae.DesulfocapsaandSulfurovumpopulations accounted for 12%–26% of sediment 16S rRNA amplicon sequences and were closely related to isolates which carry out autotrophic S⁰disproportionation in pure culture. Gibbs energy (∆G_r) calculations revealed that S⁰disproportionation under in situ conditions is energy yielding. Microsensor profiles through the mat‐sediment interface showed thatBeggiatoamats consume dissolved sulfide and oxygen, but a net increase in acidity was only observed in the sediments below. Together, these findings suggest that disproportionation is an important sink for S⁰generated by microbial sulfide oxidation in this oxygen‐limited system and may contribute to the weathering of carbonate rocks and sediments in sulfur‐rich environments.

    

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5. 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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