Distinct lactate utilization strategies drive niche differentiation between two co-existing <i>Megasphaera</i> species in the rumen microbiome

Lactate utilization mitigates rumen acidosis and is associated with decreased methane production in the rumen. While several lactate utilization pathways exist across different microbial species in the rumen, how they are metabolically differentiated remains unclear. Here, we show that the key lactate-utilizing species Megasphaera hexanoica and Megasphaera elsdenii display distinct growth strategies based on their fermentative end products. This allows them to co-exist and play distinct metabolic roles, which appear particularly relevant in the early stages of rumen development, as both species are highly enriched in the calf. Specifically, M. hexanoica is more strongly associated with rumen microbiome states that involve increased lactate utilization and preferentially runs reverse beta-oxidation (termed chain elongation) to produce butyrate and medium-chain fatty acids from lactate. As M. elsdenii instead utilizes lactate via the acrylate pathway to produce propionate, we leverage Enzyme Cost Minimization to predict how this pathway relates to a distinct growth strategy. We find that M. elsdenii maximizes growth rate when lactate transiently accumulates, which contrasts M. hexanoica's invariably high-yield strategy. This trade-off, which is supported by the analysis of growth kinetics, metabolic flux, and bioreactors simulating the rumen microbiome, ultimately contributes to co-existence on lactate and may have driven niche differentiation. Lastly, we demonstrate how lactate utilization in the Megasphaera is threatened by toxins widespread in feed, which points to dietary interventions to support calf health.

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Publication Details

Journal
The ISME Journal
Published
2025-01-01
DOI
https://doi.org/10.1093/ismejo/wraf147
Citations
4
Primary Topic
Ruminant Nutrition and Digestive Physiology
Type
article
Field-Weighted Citation Impact
7.61

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article

Distinct lactate utilization strategies drive niche differentiation between two co-existing Megasphaera species in the rumen microbiome

Viktoria Neubauer, Pieter Candry, Byung-Chul Kim, Anna J. Mueller et al.
4 citations
The ISME Journal
Ruminant Nutrition and Digestive Physiology
7.61
article

Distinct lactate utilization strategies drive niche differentiation between two co-existing Megasphaera species in the rumen microbiome

Viktoria Neubauer, Pieter Candry, Byung-Chul Kim, Anna J. Mueller, Qendrim Zebeli, Martin Wagner, Fátima C. Pereira, Johannes Faas, Cameron R. Strachan, Veronika Nagl, Christopher E. Lawson, Paul J. Weimer, Evelyne Selberherr, Xiaoqian Yu, Connor M Bowers, Martin F. Polz, Tea Movsesijan
article en
4 citations

Abstract

Lactate utilization mitigates rumen acidosis and is associated with decreased methane production in the rumen. While several lactate utilization pathways exist across different microbial species in the rumen, how they are metabolically differentiated remains unclear. Here, we show that the key lactate-utilizing species Megasphaera hexanoica and Megasphaera elsdenii display distinct growth strategies based on their fermentative end products. This allows them to co-exist and play distinct metabolic roles, which appear particularly relevant in the early stages of rumen development, as both species are highly enriched in the calf. Specifically, M. hexanoica is more strongly associated with rumen microbiome states that involve increased lactate utilization and preferentially runs reverse beta-oxidation (termed chain elongation) to produce butyrate and medium-chain fatty acids from lactate. As M. elsdenii instead utilizes lactate via the acrylate pathway to produce propionate, we leverage Enzyme Cost Minimization to predict how this pathway relates to a distinct growth strategy. We find that M. elsdenii maximizes growth rate when lactate transiently accumulates, which contrasts M. hexanoica's invariably high-yield strategy. This trade-off, which is supported by the analysis of growth kinetics, metabolic flux, and bioreactors simulating the rumen microbiome, ultimately contributes to co-existence on lactate and may have driven niche differentiation. Lastly, we demonstrate how lactate utilization in the Megasphaera is threatened by toxins widespread in feed, which points to dietary interventions to support calf health.

The ISME JournalVol. 19(1)
University of Vienna (AT), University of Wisconsin System (US), University of Wisconsin–Madison (US), University of Veterinary Medicine Vienna (AT), University of Toronto (CA), Universitätsklinikum Tulln (AT), Christian Doppler Laboratory for Thermoelectricity (AT), Landwirtschaftliche Fachschule Tulln (AT), Austrian Competence Centre of Food Safety (AT), University of Southampton (GB), Wageningen University & Research (NL)
Österreichische Nationalstiftung für Forschung, Technologie und Entwicklung, Bundesministerium für Klimaschutz, Umwelt, Energie, Mobilität, Innovation und Technologie, Bundesministerium für Wissenschaft, Forschung und Wirtschaft, Österreichische Forschungsförderungsgesellschaft, Bundesministerium für Digitalisierung und Wirtschaftsstandort, Natural Sciences and Engineering Research Council of Canada
Openalex Percentile: Top 3%
Ruminant Nutrition and Digestive Physiology
7.61
DOIOpen Access PDFOpenAlex
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