skip to main content
Explore Scholarly Publications and Datasets in the NSF-PAR

  • NSF Public Access
  • Search Results
  • Accepted Manuscript: Omics-Inferred Partitioning and Expression of Diverse Biogeochemical Functions in a Low-O 2 Cyanobacterial Mat Community
Title: Omics-Inferred Partitioning and Expression of Diverse Biogeochemical Functions in a Low-O 2 Cyanobacterial Mat Community
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 more » 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. « less
Authors:
; ; ; ; ; ;
Editors:
Bernstein, Hans C.
Award ID(s):
2046958 1637066
Publication Date:
NSF-PAR ID:
10312248
Journal Name:
mSystems
Volume:
6
Issue:
6
ISSN:
2379-5077
Sponsoring Org:
National Science Foundation
More Like this
  1. ; ; ; ; ; ; ; ; ( , 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.
  2. ; ; ; ( , 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 sourcemore »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.

    « less
  3. ; ; ; ; ; ; ; ; ( , Life)
    As we expand the search for life beyond Earth, a water-dominated planet, we turn our eyes to other aquatic worlds. Microbial life found in Earth’s many extreme habitats are considered useful analogs to life forms we are likely to find in extraterrestrial bodies of water. Modern-day benthic microbial mats inhabiting the low-oxygen, high-sulfur submerged sinkholes of temperate Lake Huron (Michigan, USA) and microbialites inhabiting the shallow, high-carbonate waters of subtropical Laguna Bacalar (Yucatan Peninsula, Mexico) serve as potential working models for exploration of extraterrestrial life. In Lake Huron, delicate mats comprising motile filaments of purple-pigmented cyanobacteria capable of oxygenic and anoxygenic photosynthesis and pigment-free chemosynthetic sulfur-oxidizing bacteria lie atop soft, organic-rich sediments. In Laguna Bacalar, lithification by cyanobacteria forms massive carbonate reef structures along the shoreline. Herein, we document studies of these two distinct earthly microbial mat ecosystems and ponder how similar or modified methods of study (e.g., robotics) would be applicable to prospective mat worlds in other planets and their moons (e.g., subsurface Mars and under-ice oceans of Europa). Further studies of modern-day microbial mat and microbialite ecosystems can add to the knowledge of Earth’s biodiversity and guide the search for life in extraterrestrial hydrospheres.
  4. ; ; ; ; ; ; ; ( , Environmental Microbiome)
    Abstract Background Lagoons are common along coastlines worldwide and are important for biogeochemical element cycling, coastal biodiversity, coastal erosion protection and blue carbon sequestration. These ecosystems are frequently disturbed by weather, tides, and human activities. Here, we investigated a shallow lagoon in New England. The brackish ecosystem releases hydrogen sulfide particularly upon physical disturbance, causing blooms of anoxygenic sulfur-oxidizing phototrophs. To study the habitat, microbial community structure, assembly and function we carried out in situ experiments investigating the bloom dynamics over time. Results Phototrophic microbial mats and permanently or seasonally stratified water columns commonly contain multiple phototrophic lineages that coexist based on their light, oxygen and nutrient preferences. We describe similar coexistence patterns and ecological niches in estuarine planktonic blooms of phototrophs. The water column showed steep gradients of oxygen, pH, sulfate, sulfide, and salinity. The upper part of the bloom was dominated by aerobic phototrophic Cyanobacteria , the middle and lower parts by anoxygenic purple sulfur bacteria ( Chromatiales ) and green sulfur bacteria ( Chlorobiales ), respectively. We show stable coexistence of phototrophic lineages from five bacterial phyla and present metagenome-assembled genomes (MAGs) of two uncultured Chlorobaculum and Prosthecochloris species. In addition to genes involved in sulfur oxidation andmore »photopigment biosynthesis the MAGs contained complete operons encoding for terminal oxidases. The metagenomes also contained numerous contigs affiliating with Microviridae viruses, potentially affecting Chlorobi . Our data suggest a short sulfur cycle within the bloom in which elemental sulfur produced by sulfide-oxidizing phototrophs is most likely reduced back to sulfide by Desulfuromonas sp . Conclusions The release of sulfide creates a habitat selecting for anoxygenic sulfur-oxidizing phototrophs, which in turn create a niche for sulfur reducers. Strong syntrophism between these guilds apparently drives a short sulfur cycle that may explain the rapid development of the bloom. The fast growth and high biomass yield of Chlorobi -affiliated organisms implies that the studied lineages of green sulfur bacteria can thrive in hypoxic habitats. This oxygen tolerance is corroborated by oxidases found in MAGs of uncultured Chlorobi . The findings improve our understanding of the ecology and ecophysiology of anoxygenic phototrophs and their impact on the coupled biogeochemical cycles of sulfur and carbon.« less
  5. ; ; ; ; ; ( , ISME)
    Blooms of planktonic cyanobacteria have long been of concern in lakes, but more recently, harmful impacts of riverine benthic cyanobacterial mats been recognized. As yet, we know little about how various benthic cyanobacteria are distributed in river networks, or how environmental conditions or other associated microbes in their consortia affect their biosynthetic capacities. We performed metagenomic sequencing for 22 Oscillatoriales-dominated (Cyanobacteria) microbial mats collected across the Eel River network in Northern California and investigated factors associated with anatoxin-a producing cyanobacteria. All microbial communities were dominated by one or two cyanobacterial species, so the key mat metabolisms involve oxygenic photosynthesis and carbon oxidation. Only a few metabolisms fueled the growth of the mat communities, with little evidence for anaerobic metabolic pathways. We genomically defined four cyanobacterial species, all which shared <96% average nucleotide identity with reference Oscillatoriales genomes and are potentially novel species in the genus Microcoleus. One of the Microcoleus species contained the anatoxin-a biosynthesis genes, and we describe the first anatoxin-a gene cluster from the Microcoleus clade within Oscillatoriales. Occurrence of these four Microcoleus species in the watershed was correlated with total dissolved nitrogen and phosphorus concentrations, and the species that contains the anatoxin-a gene cluster was found inmore »sites with higher nitrogen concentrations. Microbial assemblages in mat samples with the anatoxin-a gene cluster consistently had a lower abundance of Burkholderiales (Betaproteobacteria) species than did mats without the anatoxin-producing genes. The associations of water nutrient concentrations and certain co-occurring microbes with anatoxin-a producing Microcoleus motivate further exploration for their roles as potential controls on the distributions of toxigenic benthic cyanobacteria in river networks.« less
  • Citation Formats
  • MLA
  • APA
  • Chicago
  • BibTeX
  • Save / Share this Record
  • Send to Email