A metagenome-level analysis of a microbial community fermenting ultra-filtered milk permeate
Fermentative microbial communities have the potential to serve as biocatalysts for the conversion of low-value dairy coproducts into renewable chemicals, contributing to a more sustainable global economy. To develop predictive tools for the design and operation of industrially relevant strategies th...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-05-01
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| Series: | Frontiers in Bioengineering and Biotechnology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fbioe.2023.1173656/full |
| _version_ | 1797816525497827328 |
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| author | Kevin A. Walters Kevin A. Walters Kevin A. Walters Geethaanjali Mohan Geethaanjali Mohan Kevin S. Myers Kevin S. Myers Abel T. Ingle Abel T. Ingle Abel T. Ingle Timothy J. Donohue Timothy J. Donohue Timothy J. Donohue Daniel R. Noguera Daniel R. Noguera Daniel R. Noguera |
| author_facet | Kevin A. Walters Kevin A. Walters Kevin A. Walters Geethaanjali Mohan Geethaanjali Mohan Kevin S. Myers Kevin S. Myers Abel T. Ingle Abel T. Ingle Abel T. Ingle Timothy J. Donohue Timothy J. Donohue Timothy J. Donohue Daniel R. Noguera Daniel R. Noguera Daniel R. Noguera |
| author_sort | Kevin A. Walters |
| collection | DOAJ |
| description | Fermentative microbial communities have the potential to serve as biocatalysts for the conversion of low-value dairy coproducts into renewable chemicals, contributing to a more sustainable global economy. To develop predictive tools for the design and operation of industrially relevant strategies that utilize fermentative microbial communities, there is a need to determine the genomic features of community members that are characteristic to the accumulation of different products. To address this knowledge gap, we performed a 282-day bioreactor experiment with a microbial community that was fed ultra-filtered milk permeate, a low-value coproduct from the dairy industry. The bioreactor was inoculated with a microbial community from an acid-phase digester. A metagenomic analysis was used to assess microbial community dynamics, construct metagenome-assembled genomes (MAGs), and evaluate the potential for lactose utilization and fermentation product synthesis of community members represented by the assembled MAGs. This analysis led us to propose that, in this reactor, members of the Actinobacteriota phylum are important in the degradation of lactose, via the Leloir pathway and the bifid shunt, and the production of acetic, lactic, and succinic acids. In addition, members of the Firmicutes phylum contribute to the chain-elongation-mediated production of butyric, hexanoic, and octanoic acids, with different microbes using either lactose, ethanol, or lactic acid as the growth substrate. We conclude that genes encoding carbohydrate utilization pathways, and genes encoding lactic acid transport into the cell, electron confurcating lactate dehydrogenase, and its associated electron transfer flavoproteins, are genomic features whose presence in Firmicutes needs to be established to infer the growth substrate used for chain elongation. |
| first_indexed | 2024-03-13T08:39:58Z |
| format | Article |
| id | doaj.art-525b02b3d81a4651ad2632f757815f14 |
| institution | Directory Open Access Journal |
| issn | 2296-4185 |
| language | English |
| last_indexed | 2024-03-13T08:39:58Z |
| publishDate | 2023-05-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Bioengineering and Biotechnology |
| spelling | doaj.art-525b02b3d81a4651ad2632f757815f142023-05-30T14:55:11ZengFrontiers Media S.A.Frontiers in Bioengineering and Biotechnology2296-41852023-05-011110.3389/fbioe.2023.11736561173656A metagenome-level analysis of a microbial community fermenting ultra-filtered milk permeateKevin A. Walters0Kevin A. Walters1Kevin A. Walters2Geethaanjali Mohan3Geethaanjali Mohan4Kevin S. Myers5Kevin S. Myers6Abel T. Ingle7Abel T. Ingle8Abel T. Ingle9Timothy J. Donohue10Timothy J. Donohue11Timothy J. Donohue12Daniel R. Noguera13Daniel R. Noguera14Daniel R. Noguera15Department of Bacteriology, University of Wisconsin-Madison, Madison, WI, United StatesWisconsin Energy Institute, University of Wisconsin-Madison, Madison, WI, United StatesGreat Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, WI, United StatesWisconsin Energy Institute, University of Wisconsin-Madison, Madison, WI, United StatesGreat Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, WI, United StatesWisconsin Energy Institute, University of Wisconsin-Madison, Madison, WI, United StatesGreat Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, WI, United StatesWisconsin Energy Institute, University of Wisconsin-Madison, Madison, WI, United StatesGreat Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, WI, United StatesDepartment of Civil and Environmental Engineering, University of Wisconsin-Madison, Madison, WI, United StatesDepartment of Bacteriology, University of Wisconsin-Madison, Madison, WI, United StatesWisconsin Energy Institute, University of Wisconsin-Madison, Madison, WI, United StatesGreat Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, WI, United StatesWisconsin Energy Institute, University of Wisconsin-Madison, Madison, WI, United StatesGreat Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, WI, United StatesDepartment of Civil and Environmental Engineering, University of Wisconsin-Madison, Madison, WI, United StatesFermentative microbial communities have the potential to serve as biocatalysts for the conversion of low-value dairy coproducts into renewable chemicals, contributing to a more sustainable global economy. To develop predictive tools for the design and operation of industrially relevant strategies that utilize fermentative microbial communities, there is a need to determine the genomic features of community members that are characteristic to the accumulation of different products. To address this knowledge gap, we performed a 282-day bioreactor experiment with a microbial community that was fed ultra-filtered milk permeate, a low-value coproduct from the dairy industry. The bioreactor was inoculated with a microbial community from an acid-phase digester. A metagenomic analysis was used to assess microbial community dynamics, construct metagenome-assembled genomes (MAGs), and evaluate the potential for lactose utilization and fermentation product synthesis of community members represented by the assembled MAGs. This analysis led us to propose that, in this reactor, members of the Actinobacteriota phylum are important in the degradation of lactose, via the Leloir pathway and the bifid shunt, and the production of acetic, lactic, and succinic acids. In addition, members of the Firmicutes phylum contribute to the chain-elongation-mediated production of butyric, hexanoic, and octanoic acids, with different microbes using either lactose, ethanol, or lactic acid as the growth substrate. We conclude that genes encoding carbohydrate utilization pathways, and genes encoding lactic acid transport into the cell, electron confurcating lactate dehydrogenase, and its associated electron transfer flavoproteins, are genomic features whose presence in Firmicutes needs to be established to infer the growth substrate used for chain elongation.https://www.frontiersin.org/articles/10.3389/fbioe.2023.1173656/fullmicrobiomedairy coproductfermentationlacticsuccinicbutyric |
| spellingShingle | Kevin A. Walters Kevin A. Walters Kevin A. Walters Geethaanjali Mohan Geethaanjali Mohan Kevin S. Myers Kevin S. Myers Abel T. Ingle Abel T. Ingle Abel T. Ingle Timothy J. Donohue Timothy J. Donohue Timothy J. Donohue Daniel R. Noguera Daniel R. Noguera Daniel R. Noguera A metagenome-level analysis of a microbial community fermenting ultra-filtered milk permeate Frontiers in Bioengineering and Biotechnology microbiome dairy coproduct fermentation lactic succinic butyric |
| title | A metagenome-level analysis of a microbial community fermenting ultra-filtered milk permeate |
| title_full | A metagenome-level analysis of a microbial community fermenting ultra-filtered milk permeate |
| title_fullStr | A metagenome-level analysis of a microbial community fermenting ultra-filtered milk permeate |
| title_full_unstemmed | A metagenome-level analysis of a microbial community fermenting ultra-filtered milk permeate |
| title_short | A metagenome-level analysis of a microbial community fermenting ultra-filtered milk permeate |
| title_sort | metagenome level analysis of a microbial community fermenting ultra filtered milk permeate |
| topic | microbiome dairy coproduct fermentation lactic succinic butyric |
| url | https://www.frontiersin.org/articles/10.3389/fbioe.2023.1173656/full |
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