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Title: Dynamics of archaea at fine spatial scales in Shark Bay mat microbiomes

Abstract

Modern microbial mats provide remarkable insights into assembly, function and origin of complex microbial ecosystems. An excellent model of such systems is located in Shark Bay, Australia. Although bacteria have been extensively investigated in these communities, the role of archaea in microbial mats is poorly understood. Delineating the spatial distribution of archaea with mat depth will enable resolution of specific niches associated with this domain. In the present study, high throughput amplicon sequencing was undertaken in conjunction with key biogeochemical properties of two mat types (smooth and pustular). A total of 13,547,552 unfiltered sequences were obtained, and classified sequences were affiliated to three archaeal and candidate phyla, Parvarchaeota, Euryarchaeota and Crenarchaeota. One way analysis of similarity tests (ANOSIM) indicated the archaeal community structures of smooth and pustular mats were significantly different (global R = 1, p = 0.1 %). Smooth mats possessed higher archaeal diversity, dominated by Parvarchaeota, followed by Thermoplasmata, Class marine benthic group B and Halobacteria. The methanogenic community in smooth mats was dominated by hydrogenotrophic Methanomicrobiales, as well as methylotrophic Methanosarcinales, Methanococcales, Methanobacteriales and Methanomassiliicoccaceae. Conversely, pustular mats were enriched with Halobacteria and Parvarchaeota. The rates of oxygen production/consumption as well as sulphate reduction were up tomore » four times higher in smooth than in pustular mats. Methane production peaked in the oxic part of mats and was up to seven-fold higher in smooth than in pustular mats. Metabolic cooperation in putative surface anoxic niches is proposed to be key in efficient cycling of key nutrients in these systems.« less

Authors:
 [1];  [2];  [3];  [1];  [4];  [1]
  1. The Univ. of New South Wales, Sydney (Australia)
  2. Univ. of Connecticut, Storrs, CT (United States); Univ. of New South Wales, Sydney (Australia)
  3. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  4. Univ. of Connecticut, Storrs, CT (United States)
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1358501
Report Number(s):
PNNL-SA-120053
Journal ID: ISSN 2045-2322
Grant/Contract Number:
AC05-76RL01830
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Scientific Reports
Additional Journal Information:
Journal Volume: 7; Journal ID: ISSN 2045-2322
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; archaea; microbial ecology

Citation Formats

Wong, Hon Lun, Visscher, Pieter T., White, III, Richard Allen, Smith, Daniela -Lee, Patterson, Molly M., and Burns, Brendan P.. Dynamics of archaea at fine spatial scales in Shark Bay mat microbiomes. United States: N. p., 2017. Web. doi:10.1038/srep46160.
Wong, Hon Lun, Visscher, Pieter T., White, III, Richard Allen, Smith, Daniela -Lee, Patterson, Molly M., & Burns, Brendan P.. Dynamics of archaea at fine spatial scales in Shark Bay mat microbiomes. United States. doi:10.1038/srep46160.
Wong, Hon Lun, Visscher, Pieter T., White, III, Richard Allen, Smith, Daniela -Lee, Patterson, Molly M., and Burns, Brendan P.. Tue . "Dynamics of archaea at fine spatial scales in Shark Bay mat microbiomes". United States. doi:10.1038/srep46160. https://www.osti.gov/servlets/purl/1358501.
@article{osti_1358501,
title = {Dynamics of archaea at fine spatial scales in Shark Bay mat microbiomes},
author = {Wong, Hon Lun and Visscher, Pieter T. and White, III, Richard Allen and Smith, Daniela -Lee and Patterson, Molly M. and Burns, Brendan P.},
abstractNote = {Modern microbial mats provide remarkable insights into assembly, function and origin of complex microbial ecosystems. An excellent model of such systems is located in Shark Bay, Australia. Although bacteria have been extensively investigated in these communities, the role of archaea in microbial mats is poorly understood. Delineating the spatial distribution of archaea with mat depth will enable resolution of specific niches associated with this domain. In the present study, high throughput amplicon sequencing was undertaken in conjunction with key biogeochemical properties of two mat types (smooth and pustular). A total of 13,547,552 unfiltered sequences were obtained, and classified sequences were affiliated to three archaeal and candidate phyla, Parvarchaeota, Euryarchaeota and Crenarchaeota. One way analysis of similarity tests (ANOSIM) indicated the archaeal community structures of smooth and pustular mats were significantly different (global R = 1, p = 0.1 %). Smooth mats possessed higher archaeal diversity, dominated by Parvarchaeota, followed by Thermoplasmata, Class marine benthic group B and Halobacteria. The methanogenic community in smooth mats was dominated by hydrogenotrophic Methanomicrobiales, as well as methylotrophic Methanosarcinales, Methanococcales, Methanobacteriales and Methanomassiliicoccaceae. Conversely, pustular mats were enriched with Halobacteria and Parvarchaeota. The rates of oxygen production/consumption as well as sulphate reduction were up to four times higher in smooth than in pustular mats. Methane production peaked in the oxic part of mats and was up to seven-fold higher in smooth than in pustular mats. Metabolic cooperation in putative surface anoxic niches is proposed to be key in efficient cycling of key nutrients in these systems.},
doi = {10.1038/srep46160},
journal = {Scientific Reports},
number = ,
volume = 7,
place = {United States},
year = {Tue Apr 11 00:00:00 EDT 2017},
month = {Tue Apr 11 00:00:00 EDT 2017}
}

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  • Modern microbial mats are potential analogues of some of Earth’s earliest ecosystems. Excellent examples can be found in Shark Bay, Australia, with mats of various morphologies. To further our understanding of the functional genetic potential of these complex microbial ecosystems, we conducted for the first time shotgun metagenomic analyses. We assembled metagenomic nextgeneration sequencing data to classify the taxonomic and metabolic potential across diverse morphologies of marine mats in Shark Bay. The microbial community across taxonomic classifications using protein-coding and small subunit rRNA genes directly extracted from the metagenomes suggests that three phyla Proteobacteria, Cyanobacteria and Bacteriodetes dominate all marinemore » mats. However, the microbial community structure between Shark Bay and Highbourne Cay (Bahamas) marine systems appears to be distinct from each other. The metabolic potential (based on SEED subsystem classifications) of the Shark Bay and Highbourne Cay microbial communities were also distinct. Shark Bay metagenomes have a metabolic pathway profile consisting of both heterotrophic and photosynthetic pathways, whereas Highbourne Cay appears to be dominated almost exclusively by photosynthetic pathways. Alternative non-rubisco-based carbon metabolism including reductive TCA cycle and 3-hydroxypropionate/4-hydroxybutyrate pathways is highly represented in Shark Bay metagenomes while not represented in Highbourne Cay microbial mats or any other mat forming ecosystems investigated to date. Potentially novel aspects of nitrogen cycling were also observed, as well as putative heavy metal cycling (arsenic, mercury, copper and cadmium). Finally, archaea are highly represented in Shark Bay and may have critical roles in overall ecosystem function in these modern microbial mats.« less
  • Phototrophic mat communities are model ecosystems for studying energy cycling and elemental transformations because complete biogeochemical cycles occur over millimeter-to-centimeter scales. Characterization of energy and nutrient capture within hypersaline phototrophic mats has focused on specific processes and organisms, however little is known about community-wide distribution of and linkages between these processes. To investigate energy and macronutrient capture and flow through a structured community, the spatial and organismal distribution of metabolic functions within a compact hypersaline mat community from Hot Lake have been broadly elucidated through species-resolved metagenomics and geochemical, microbial diversity, and metabolic gradient measurements. Draft reconstructed genomes of abundantmore » organisms revealed three dominant cyanobacterial populations differentially distributed across the top layers of the mat suggesting niche separation along light and oxygen gradients. Many organisms contained diverse functional profiles, allowing for metabolic response to changing conditions within the mat. Organisms with partial nitrogen and sulfur metabolisms were widespread indicating dependence upon metabolite exchange. In addition, changes in community spatial structure were observed over the diel. These results indicate that organisms within the mat community have adapted to the temporally dynamic environmental gradients in this hypersaline mat through metabolic flexibility and fluid syntrophic interactions, including shifts in spatial arrangements.« less
  • Subsurface zones of groundwater and surface water mixing (hyporheic zones) are regions of enhanced rates of biogeochemical cycling, yet ecological processes governing hyporheic microbiome composition and function through space and time remain unknown. We sampled attached and planktonic microbiomes in the Columbia River hyporheic zone across seasonal hydrologic change, and employed statistical null models to infer mechanisms generating temporal changes in microbiomes within three hydrologically-connected, physicochemically-distinct geographic zones (inland, nearshore, river). We reveal that microbiomes remain dissimilar through time across all zones and habitat types (attached vs. planktonic) and that deterministic assembly processes regulate microbiome composition in all data subsets.more » The consistent presence of heterotrophic taxa and members of the Planctomycetes-Verrucomicrobia-Chlamydiae (PVC) superphylum nonetheless suggests common selective pressures for physiologies represented in these groups. Further, co-occurrence networks were used to provide insight into taxa most affected by deterministic assembly processes. We identified network clusters to represent groups of organisms that correlated with seasonal and physicochemical change. Extended network analyses identified keystone taxa within each cluster that we propose are central in microbiome composition and function. Finally, the abundance of one network cluster of nearshore organisms exhibited a seasonal shift from heterotrophic to autotrophic metabolisms and correlated with microbial metabolism, possibly indicating an ecological role for these organisms as foundational species in driving biogeochemical reactions within the hyporheic zone. Taken together, our research demonstrates a predominant role for deterministic assembly across highly-connected environments and provides insight into niche dynamics associated with seasonal changes in hyporheic microbiome composition and metabolism.« less
  • The study of natural archaeal assemblages requires community context, namely, a concurrent assessment of the dynamics of archaeal, bacterial, and viral populations. Here, we use filter size-resolved metagenomic analyses to report the dynamics of 101 archaeal and bacterial OTUs and 140 viral populations across 17 samples collected over different timescales from 2007–2010 from Australian hypersaline Lake Tyrrell (LT). All samples were dominated by Archaea (75–95%). Archaeal, bacterial, and viral populations were found to be dynamic on timescales of months to years, and different viral assemblages were present in planktonic, relative to host-associated (active and provirus) size fractions. Analyses of clusteredmore » regularly interspaced short palindromic repeat (CRISPR) regions indicate that both rare and abundant viruses were targeted, primarily by lower abundance hosts. Although very few spacers had hits to the NCBI nr database or to the 140 LT viral populations, 21% had hits to unassembled LT viral concentrate reads. This suggests local adaptation to LT-specific viruses and/or undersampling of haloviral assemblages in public databases, along with successful CRISPR-mediated maintenance of viral populations at abundances low enough to preclude genomic assembly. This is the first metagenomic report evaluating widespread archaeal dynamics at the population level on short timescales in a hypersaline system.« less
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