Vitamin and Amino Acid Auxotrophy in Anaerobic Consortia Operating under Methanogenic Conditions

ABSTRACT Syntrophy among Archaea and Bacteria facilitates the anaerobic degradation of organic compounds to CH4 and CO2. Particularly during aliphatic and aromatic hydrocarbon mineralization, as in the case of crude oil reservoirs and petroleum-contaminated sediments, metabolic interactions between...

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Autores principales: Valerie Hubalek, Moritz Buck, BoonFei Tan, Julia Foght, Annelie Wendeberg, David Berry, Stefan Bertilsson, Alexander Eiler
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Publicado: American Society for Microbiology 2017
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spelling oai:doaj.org-article:d3a9074bbcd54a78b2bb36e5abe83a0b2021-12-02T18:15:43ZVitamin and Amino Acid Auxotrophy in Anaerobic Consortia Operating under Methanogenic Conditions10.1128/mSystems.00038-172379-5077https://doaj.org/article/d3a9074bbcd54a78b2bb36e5abe83a0b2017-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00038-17https://doaj.org/toc/2379-5077ABSTRACT Syntrophy among Archaea and Bacteria facilitates the anaerobic degradation of organic compounds to CH4 and CO2. Particularly during aliphatic and aromatic hydrocarbon mineralization, as in the case of crude oil reservoirs and petroleum-contaminated sediments, metabolic interactions between obligate mutualistic microbial partners are of central importance. Using micromanipulation combined with shotgun metagenomic approaches, we describe the genomes of complex consortia within short-chain alkane-degrading cultures operating under methanogenic conditions. Metabolic reconstruction revealed that only a small fraction of genes in the metagenome-assembled genomes encode the capacity for fermentation of alkanes facilitated by energy conservation linked to H2 metabolism. Instead, the presence of inferred lifestyles based on scavenging anabolic products and intermediate fermentation products derived from detrital biomass was a common feature. Additionally, inferred auxotrophy for vitamins and amino acids suggests that the hydrocarbon-degrading microbial assemblages are structured and maintained by multiple interactions beyond the canonical H2-producing and syntrophic alkane degrader-methanogen partnership. Compared to previous work, our report points to a higher order of complexity in microbial consortia engaged in anaerobic hydrocarbon transformation. IMPORTANCE Microbial interactions between Archaea and Bacteria mediate many important chemical transformations in the biosphere from degrading abundant polymers to synthesis of toxic compounds. Two of the most pressing issues in microbial interactions are how consortia are established and how we can modulate these microbial communities to express desirable functions. Here, we propose that public goods (i.e., metabolites of high energy demand in biosynthesis) facilitate energy conservation for life under energy-limited conditions and determine the assembly and function of the consortia. Our report suggests that an understanding of public good dynamics could result in new ways to improve microbial pollutant degradation in anaerobic systems.Valerie HubalekMoritz BuckBoonFei TanJulia FoghtAnnelie WendebergDavid BerryStefan BertilssonAlexander EilerAmerican Society for MicrobiologyarticleBlack Queen hypothesismetagenomicspetroleumsyntrophyMicrobiologyQR1-502ENmSystems, Vol 2, Iss 5 (2017)
institution DOAJ
collection DOAJ
language EN
topic Black Queen hypothesis
metagenomics
petroleum
syntrophy
Microbiology
QR1-502
spellingShingle Black Queen hypothesis
metagenomics
petroleum
syntrophy
Microbiology
QR1-502
Valerie Hubalek
Moritz Buck
BoonFei Tan
Julia Foght
Annelie Wendeberg
David Berry
Stefan Bertilsson
Alexander Eiler
Vitamin and Amino Acid Auxotrophy in Anaerobic Consortia Operating under Methanogenic Conditions
description ABSTRACT Syntrophy among Archaea and Bacteria facilitates the anaerobic degradation of organic compounds to CH4 and CO2. Particularly during aliphatic and aromatic hydrocarbon mineralization, as in the case of crude oil reservoirs and petroleum-contaminated sediments, metabolic interactions between obligate mutualistic microbial partners are of central importance. Using micromanipulation combined with shotgun metagenomic approaches, we describe the genomes of complex consortia within short-chain alkane-degrading cultures operating under methanogenic conditions. Metabolic reconstruction revealed that only a small fraction of genes in the metagenome-assembled genomes encode the capacity for fermentation of alkanes facilitated by energy conservation linked to H2 metabolism. Instead, the presence of inferred lifestyles based on scavenging anabolic products and intermediate fermentation products derived from detrital biomass was a common feature. Additionally, inferred auxotrophy for vitamins and amino acids suggests that the hydrocarbon-degrading microbial assemblages are structured and maintained by multiple interactions beyond the canonical H2-producing and syntrophic alkane degrader-methanogen partnership. Compared to previous work, our report points to a higher order of complexity in microbial consortia engaged in anaerobic hydrocarbon transformation. IMPORTANCE Microbial interactions between Archaea and Bacteria mediate many important chemical transformations in the biosphere from degrading abundant polymers to synthesis of toxic compounds. Two of the most pressing issues in microbial interactions are how consortia are established and how we can modulate these microbial communities to express desirable functions. Here, we propose that public goods (i.e., metabolites of high energy demand in biosynthesis) facilitate energy conservation for life under energy-limited conditions and determine the assembly and function of the consortia. Our report suggests that an understanding of public good dynamics could result in new ways to improve microbial pollutant degradation in anaerobic systems.
format article
author Valerie Hubalek
Moritz Buck
BoonFei Tan
Julia Foght
Annelie Wendeberg
David Berry
Stefan Bertilsson
Alexander Eiler
author_facet Valerie Hubalek
Moritz Buck
BoonFei Tan
Julia Foght
Annelie Wendeberg
David Berry
Stefan Bertilsson
Alexander Eiler
author_sort Valerie Hubalek
title Vitamin and Amino Acid Auxotrophy in Anaerobic Consortia Operating under Methanogenic Conditions
title_short Vitamin and Amino Acid Auxotrophy in Anaerobic Consortia Operating under Methanogenic Conditions
title_full Vitamin and Amino Acid Auxotrophy in Anaerobic Consortia Operating under Methanogenic Conditions
title_fullStr Vitamin and Amino Acid Auxotrophy in Anaerobic Consortia Operating under Methanogenic Conditions
title_full_unstemmed Vitamin and Amino Acid Auxotrophy in Anaerobic Consortia Operating under Methanogenic Conditions
title_sort vitamin and amino acid auxotrophy in anaerobic consortia operating under methanogenic conditions
publisher American Society for Microbiology
publishDate 2017
url https://doaj.org/article/d3a9074bbcd54a78b2bb36e5abe83a0b
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AT anneliewendeberg vitaminandaminoacidauxotrophyinanaerobicconsortiaoperatingundermethanogenicconditions
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