Can rumen bacteria communicate to each other?

Mi-Young Won,Linda B Oyama,Stephen J Courtney,Sharon A Huws,Christopher J Creevey

doi:10.1186/s40168-020-00796-y

Abstract

BackgroundThe rumen contains a myriad of microbes whose primary role is to degrade and ferment dietary nutrients, which then provide the host with energy and nutrients. Rumen microbes commonly attach to ingested plant materials and form biofilms for effective plant degradation. Quorum sensing (QS) is a well-recognised form of bacterial communication in most biofilm communities, with homoserine lactone (AHL)-based QS commonly being used by Gram-negative bacteria alone and AI-2 Lux-based QS communication being used to communicate across Gram-negative and Gram-positive bacteria. However, bacterial cell to cell communication in the rumen is poorly understood. In this study, rumen bacterial genomes from the Hungate collection and Genbank were prospected for QS-related genes. To check that the discovered QS genes are actually expressed in the rumen, we investigated expression levels in rumen metatranscriptome datasets.ResultsA total of 448 rumen bacterial genomes from the Hungate collection and Genbank, comprised of 311 Gram-positive, 136 Gram-negative and 1 Gram stain variable bacterium, were analysed. Abundance and distribution of AHL and AI-2 signalling genes showed that only one species (Citrobacter sp. NLAE-zl-C269) of a Gram-negative bacteria appeared to possess an AHL synthase gene, while the Lux-based genes (AI-2 QS) were identified in both Gram-positive and Gram-positive bacteria (191 genomes representing 38.2% of total genomes). Of these 192 genomes, 139 are from Gram-positive bactreetteria and 53 from Gram-negative bacteria. We also found that the genera Butyrivibrio, Prevotella, Ruminococcus and Pseudobutyrivibrio, which are well known as the most abundant bacterial genera in the rumen, possessed the most lux-based AI-2 QS genes. Gene expression levels within the metatranscriptome dataset showed that Prevotella, in particular, expressed high levels of LuxS synthase suggesting that this genus plays an important role in QS within the rumen.ConclusionThis is the most comprehensive study of QS in the rumen microbiome to date. This study shows that AI-2-based QS is rife in the rumen. These results allow a greater understanding on plant-microbe interactions in the rumen.

Highlights

The rumen contains a myriad of microbes whose primary role is to degrade and ferment dietary nutrients, which provide the host with energy and nutrients
Quorum sensing-related proteins with rumen bacterial genomes For the purpose of analysis, two genera, Lachnobacterium and Micrococcus, which are often described as weakly Gram-positive or Gram-variable respectively were included with the Gram-positive bacteria group (Additional file 1: Table S1)
When specific species names or strain ID could not be identified from Genbank genome entries, results were included with closely related genera or families in the Hungate collection

Summary

Introduction

The rumen contains a myriad of microbes whose primary role is to degrade and ferment dietary nutrients, which provide the host with energy and nutrients. Even though the rumen microbiome has been studied for many years, progress in understanding rumen microbial function has been slow due to the complexity of the ecosystem and available technologies, recent ‘omic advances have (2020) 8:23 bacteria, upregulation of QS autoinducer chemicals, followed by receptor binding, instigates changes in overall bacterial gene expression and phenotype, with increased virulence commonly being a consequence [4]. Erikson et al (2002) [5] were not able to identify which bacteria produce AHL using Gram-negative rumen bacterial pure cultures, including Anaerovibrio lipolyticus 5S, Fibrobacter succinogenes S85, Megasphaera elsdenii LC1, Prevotella albensis 223/M2/7, P. brevis GA33, P. bryantii B14, P. ruminocola 23 and B85, Ruminobacter amylophilus 70 and WP109, Selenomonas ruminantium HD4, four unnamed S. ruminantium strains and Succinovibrio dextrinosolvens 24, as well as Gram-positive ruminal pure culture bacteria Butyrivibrio fibrisolvens, Lachnospira multiparus 20, Ruminococcus albus B199, two strains of R. flavefaciens and Streptococcus bovis YM150 This suggests that the as yet unculturable bacteria or other cultured bacteria not tested by Erickson et al (2002) [5] may be responsible for most of the AHL signals found in rumen fluid. Mitsumori and colleagues (2003) [10] detected AI-2 signals in pure cultures of B. fibrisolvens, Eubacterium ruminantium, Ruminococcus flavefaciens and Succinomonas amylolytica, suggesting a prominent role of AI-2-based QS in the rumen

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