Strachan Cameron R, Bowers Connor M, Kim Byung-Chul, Movsesijan Tea, Neubauer Viktoria, Mueller Anna J, Yu Xiaoqian A, Pereira Fátima C, Nagl Veronika, Faas Johannes, Wagner Martin, Zebeli Qendrim, Weimer Paul J, Candry Pieter, Polz Martin F, Lawson Christopher E, Selberherr Evelyne
Centre for Food Science and Veterinary Public Health, Clinical Department for Farm Animals and Food System Science, University of Veterinary Medicine Vienna, Veterinärplatz 1, Vienna 1210, Austria.
FFoQSI GmbH - Austrian Competence Centre for Feed and Food Quality, Safety and Innovation, Technopark 1D, Tulln 3430, Austria.
ISME J. 2025 Jan 2;19(1). doi: 10.1093/ismejo/wraf147.
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.
乳酸利用可减轻瘤胃酸中毒，并与瘤胃中甲烷产量的降低有关。虽然瘤胃中不同微生物物种存在多种乳酸利用途径，但它们在代谢上如何分化仍不清楚。在这里，我们表明关键的乳酸利用物种己酸巨球形菌和埃氏巨球形菌根据其发酵终产物表现出不同的生长策略。这使它们能够共存并发挥不同的代谢作用，这在瘤胃发育的早期阶段似乎尤为重要，因为这两个物种在犊牛中都高度富集。具体而言，己酸巨球形菌与涉及乳酸利用增加的瘤胃微生物群状态更密切相关，并优先进行逆向β-氧化（称为链延长），以从乳酸中产生丁酸和中链脂肪酸。由于埃氏巨球形菌通过丙烯酸途径利用乳酸来产生丙酸，我们利用酶成本最小化来预测该途径与独特生长策略的关系。我们发现，当乳酸短暂积累时，埃氏巨球形菌的生长速率最大化，这与己酸巨球形菌始终高产的策略形成对比。这种权衡得到了生长动力学、代谢通量和模拟瘤胃微生物群的生物反应器分析的支持，最终有助于在乳酸上共存，并可能推动了生态位分化。最后，我们证明了巨球形菌中的乳酸利用如何受到饲料中广泛存在的毒素的威胁，这指出了支持犊牛健康的饮食干预措施。
