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Microbial communities mediating algal detritus turnover under anaerobic conditions

BACKGROUND: Algae encompass a wide array of photosynthetic organisms that are ubiquitously distributed in aquatic and terrestrial habitats. Algal species often bloom in aquatic ecosystems, providing a significant autochthonous carbon input to the deeper anoxic layers in stratified water bodies. In a...

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Autores principales: Morrison, Jessica M., Murphy, Chelsea L., Baker, Kristina, Zamor, Richard M., Nikolai, Steve J., Wilder, Shawn, Elshahed, Mostafa S., Youssef, Noha H.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: PeerJ Inc. 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5228501/
https://www.ncbi.nlm.nih.gov/pubmed/28097050
http://dx.doi.org/10.7717/peerj.2803
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author Morrison, Jessica M.
Murphy, Chelsea L.
Baker, Kristina
Zamor, Richard M.
Nikolai, Steve J.
Wilder, Shawn
Elshahed, Mostafa S.
Youssef, Noha H.
author_facet Morrison, Jessica M.
Murphy, Chelsea L.
Baker, Kristina
Zamor, Richard M.
Nikolai, Steve J.
Wilder, Shawn
Elshahed, Mostafa S.
Youssef, Noha H.
author_sort Morrison, Jessica M.
collection PubMed
description BACKGROUND: Algae encompass a wide array of photosynthetic organisms that are ubiquitously distributed in aquatic and terrestrial habitats. Algal species often bloom in aquatic ecosystems, providing a significant autochthonous carbon input to the deeper anoxic layers in stratified water bodies. In addition, various algal species have been touted as promising candidates for anaerobic biogas production from biomass. Surprisingly, in spite of its ecological and economic relevance, the microbial community involved in algal detritus turnover under anaerobic conditions remains largely unexplored. RESULTS: Here, we characterized the microbial communities mediating the degradation of Chlorella vulgaris (Chlorophyta), Chara sp. strain IWP1 (Charophyceae), and kelp Ascophyllum nodosum (phylum Phaeophyceae), using sediments from an anaerobic spring (Zodlteone spring, OK; ZDT), sludge from a secondary digester in a local wastewater treatment plant (Stillwater, OK; WWT), and deeper anoxic layers from a seasonally stratified lake (Grand Lake O’ the Cherokees, OK; GL) as inoculum sources. Within all enrichments, the majority of algal biomass was metabolized within 13–16 weeks, and the process was accompanied by an increase in cell numbers and a decrease in community diversity. Community surveys based on the V4 region of the 16S rRNA gene identified different lineages belonging to the phyla Bacteroidetes, Proteobacteria (alpha, delta, gamma, and epsilon classes), Spirochaetes, and Firmicutes that were selectively abundant under various substrate and inoculum conditions. Within all kelp enrichments, the microbial communities structures at the conclusion of the experiment were highly similar regardless of the enrichment source, and were dominated by the genus Clostridium, or family Veillonellaceae within the Firmicutes. In all other enrichments the final microbial community was dependent on the inoculum source, rather than the type of algae utilized as substrate. Lineages enriched included the uncultured groups VadinBC27 and WCHB1-69 within the Bacteroidetes, genus Spirochaeta and the uncultured group SHA-4 within Spirochaetes, Ruminococcaceae, Lachnospiraceae, Yongiibacter, Geosporobacter, and Acidaminobacter within the Firmicutes, and genera Kluyvera, Pantoea, Edwardsiella and Aeromonas, and Buttiauxella within the Gamma-Proteobaceteria order Enterobacteriales. CONCLUSIONS: Our results represent the first systematic survey of microbial communities mediating turnover of algal biomass under anaerobic conditions, and highlights the diversity of lineages putatively involved in the degradation process.
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spelling pubmed-52285012017-01-17 Microbial communities mediating algal detritus turnover under anaerobic conditions Morrison, Jessica M. Murphy, Chelsea L. Baker, Kristina Zamor, Richard M. Nikolai, Steve J. Wilder, Shawn Elshahed, Mostafa S. Youssef, Noha H. PeerJ Microbiology BACKGROUND: Algae encompass a wide array of photosynthetic organisms that are ubiquitously distributed in aquatic and terrestrial habitats. Algal species often bloom in aquatic ecosystems, providing a significant autochthonous carbon input to the deeper anoxic layers in stratified water bodies. In addition, various algal species have been touted as promising candidates for anaerobic biogas production from biomass. Surprisingly, in spite of its ecological and economic relevance, the microbial community involved in algal detritus turnover under anaerobic conditions remains largely unexplored. RESULTS: Here, we characterized the microbial communities mediating the degradation of Chlorella vulgaris (Chlorophyta), Chara sp. strain IWP1 (Charophyceae), and kelp Ascophyllum nodosum (phylum Phaeophyceae), using sediments from an anaerobic spring (Zodlteone spring, OK; ZDT), sludge from a secondary digester in a local wastewater treatment plant (Stillwater, OK; WWT), and deeper anoxic layers from a seasonally stratified lake (Grand Lake O’ the Cherokees, OK; GL) as inoculum sources. Within all enrichments, the majority of algal biomass was metabolized within 13–16 weeks, and the process was accompanied by an increase in cell numbers and a decrease in community diversity. Community surveys based on the V4 region of the 16S rRNA gene identified different lineages belonging to the phyla Bacteroidetes, Proteobacteria (alpha, delta, gamma, and epsilon classes), Spirochaetes, and Firmicutes that were selectively abundant under various substrate and inoculum conditions. Within all kelp enrichments, the microbial communities structures at the conclusion of the experiment were highly similar regardless of the enrichment source, and were dominated by the genus Clostridium, or family Veillonellaceae within the Firmicutes. In all other enrichments the final microbial community was dependent on the inoculum source, rather than the type of algae utilized as substrate. Lineages enriched included the uncultured groups VadinBC27 and WCHB1-69 within the Bacteroidetes, genus Spirochaeta and the uncultured group SHA-4 within Spirochaetes, Ruminococcaceae, Lachnospiraceae, Yongiibacter, Geosporobacter, and Acidaminobacter within the Firmicutes, and genera Kluyvera, Pantoea, Edwardsiella and Aeromonas, and Buttiauxella within the Gamma-Proteobaceteria order Enterobacteriales. CONCLUSIONS: Our results represent the first systematic survey of microbial communities mediating turnover of algal biomass under anaerobic conditions, and highlights the diversity of lineages putatively involved in the degradation process. PeerJ Inc. 2017-01-10 /pmc/articles/PMC5228501/ /pubmed/28097050 http://dx.doi.org/10.7717/peerj.2803 Text en ©2017 Morrison et al. http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.
spellingShingle Microbiology
Morrison, Jessica M.
Murphy, Chelsea L.
Baker, Kristina
Zamor, Richard M.
Nikolai, Steve J.
Wilder, Shawn
Elshahed, Mostafa S.
Youssef, Noha H.
Microbial communities mediating algal detritus turnover under anaerobic conditions
title Microbial communities mediating algal detritus turnover under anaerobic conditions
title_full Microbial communities mediating algal detritus turnover under anaerobic conditions
title_fullStr Microbial communities mediating algal detritus turnover under anaerobic conditions
title_full_unstemmed Microbial communities mediating algal detritus turnover under anaerobic conditions
title_short Microbial communities mediating algal detritus turnover under anaerobic conditions
title_sort microbial communities mediating algal detritus turnover under anaerobic conditions
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5228501/
https://www.ncbi.nlm.nih.gov/pubmed/28097050
http://dx.doi.org/10.7717/peerj.2803
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