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Metagenomic, (bio)chemical, and microscopic analyses reveal the potential for the cycling of sulfated EPS in Shark Bay pustular mats

Skoog, Emilie J. and Moore, Kelsey R. and Gong, Jian and Ciccarese, Davide and Momper, Lily and Cutts, Elise M. and Bosak, Tanja (2022) Metagenomic, (bio)chemical, and microscopic analyses reveal the potential for the cycling of sulfated EPS in Shark Bay pustular mats. ISME Communications, 2 . Art. No. 43. ISSN 2730-6151. doi:10.1038/s43705-022-00128-1. https://resolver.caltech.edu/CaltechAUTHORS:20220520-511985000

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Abstract

Cyanobacteria and extracellular polymeric substances (EPS) in peritidal pustular microbial mats have a two-billion-year-old fossil record. To understand the composition, production, degradation, and potential role of EPS in modern analogous communities, we sampled pustular mats from Shark Bay, Australia and analyzed their EPS matrix. Biochemical and microscopic analyses identified sulfated organic compounds as major components of mat EPS. Sulfur was more abundant in the unmineralized regions with cyanobacteria and less prevalent in areas that contained fewer cyanobacteria and more carbonate precipitates. Sequencing and assembly of the pustular mat sample resulted in 83 high-quality metagenome-assembled genomes (MAGs). Metagenomic analyses confirmed cyanobacteria as the primary sources of these sulfated polysaccharides. Genes encoding for sulfatases, glycosyl hydrolases, and other enzymes with predicted roles in the degradation of sulfated polysaccharides were detected in the MAGs of numerous clades including Bacteroidetes, Chloroflexi, Hydrogenedentes, Myxococcota, Verrucomicrobia, and Planctomycetes. Measurable sulfatase activity in pustular mats and fresh cyanobacterial EPS confirmed the role of sulfatases in the degradation of sulfated EPS. These findings suggest that the synthesis, modification, and degradation of sulfated polysaccharides influence microbial interactions, carbon cycling, and biomineralization processes within peritidal pustular microbial mats.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1038/s43705-022-00128-1DOIArticle
ORCID:
AuthorORCID
Skoog, Emilie J.0000-0003-2370-8717
Gong, Jian0000-0001-7214-1628
Ciccarese, Davide0000-0001-5505-5103
Momper, Lily0000-0002-1069-681X
Cutts, Elise M.0000-0001-7913-2417
Bosak, Tanja0000-0001-5179-5323
Additional Information:© The Author(s) 2022. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Received 27 March 2022. Revised 12 April 2022. Accepted 27 April 2022. Published 19 May 2022. The authors thank the Simons Foundation for funding this work through grants to Tanja Bosak (#327126 and #344707). This work made use of the Shared Experimental Facilities supported in part by the MRSEC Program of the National Science Foundation under award number DMR-1419807. We thank Dave Holley and the Fenney family for sampling support. We are further grateful to Sarah Hu for guidance in R programming and to James Hall and Matthew Baldes for data acquisition support. Contributions. EJS and TB conceived and designed this study. KRM, LM, and TB acquired pustular mat samples. KRM assisted in embedding samples for thin sectioning, extracting EPS, analyzing samples with FT-IR, and performing the toluidine blue assay. JG created the thin sections, visualized them with SEM, and stitched the resulting SEM image. JG and DC acquired and analyzed confocal image data. DC developed scripts to select the ROI in the SEM-EDS images and map the intensities in each pixel for each element of interest within the ROI. KRM and LM extracted DNA and sequenced the pustular mats, and LM assembled and binned MAGs. EJS performed quality control, taxonomy assignment, and annotation for all MAGs. EMC analyzed MAGs for the presence of carrageenan sulfatases. EJS performed all other data acquisition and analysis. EJS wrote the manuscript with input from all authors. The authors declare no competing interests.
Funders:
Funding AgencyGrant Number
Simons Foundation327126
Simons Foundation344707
NSFDMR-1419807
DOI:10.1038/s43705-022-00128-1
Record Number:CaltechAUTHORS:20220520-511985000
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20220520-511985000
Official Citation:Skoog, E.J., Moore, K.R., Gong, J. et al. Metagenomic, (bio)chemical, and microscopic analyses reveal the potential for the cycling of sulfated EPS in Shark Bay pustular mats. ISME COMMUN. 2, 43 (2022). https://doi.org/10.1038/s43705-022-00128-1
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:114819
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:20 May 2022 20:18
Last Modified:20 May 2022 20:18

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