反刍动物瘤胃微生物LuxS/AI-2群体感应研究进展

doi:10.11843/j.issn.0366-6964.2024.05.008

摘要/Abstract

摘要： 群体感应(quorum sensing, QS)是细菌利用信号分子进行种内或种间交流的一种通讯机制，借助该通讯机制微生物群体可以实现微生物个体无法完成的生理功能或行为调节，如生物膜形成、毒素分泌和生物发光等，以增强对外界胁迫环境的适应性。近期多组学研究发现，以自体诱导物-2(autoinducer-2, AI-2)为信号分子、LuxS为调节蛋白介导的LuxS/AI-2 QS是瘤胃微生物之间交流的主要通讯机制，影响着瘤胃微生物对饲料的利用效率。本文从AI-2的化学结构和转导途径对微生物LuxS/AI-2 QS进行总结，对LuxS/AI--2 QS在反刍动物瘤胃微生物定殖和饲料消化过程中的作用进行综述，并对LuxS/AI-2 QS在饲料消化、应激调控中的潜在作用进行展望，以期为通过LuxS/AI-2 QS调控瘤胃微生物消化代谢和稳态的生产策略提供理论参考。

关键词: LuxS/AI-2群体感应, 生物膜, 瘤胃微生物, 群落稳定性, 饲料消化

Abstract: Quorum sensing (QS) is a communication mechanism utilized by bacteria to facilitate intra-species or inter-species communication through the signaling molecules. Through this communication mechanism, microorganisms can collectively conduct physiological functions or regulate behaviors that cannot be achieved by microbial individual. These functions include biofilm formation, toxin secretion, bioluminescence, and other adaptive responses to enhance the adaptability of microorganisms against external stress environment. Recently, multi-omics studies have revealed that LuxS/AI-2 QS, mediated by the autoinducer-2 (AI-2) signaling molecule and regulated by the LuxS protein, serves as the primary communication mechanism among rumen microbe, influencing their efficiency in feed utilization. This review provides a summary of the LuxS/AI-2 QS in rumen microbe, focusing on the chemical structure of AI-2 and its transduction pathways. The roles of LuxS/AI-2 QS in rumen microbial colonization and feed digestion in ruminants were reviewed, as well as the potential roles of LuxS/AI-2 QS in feed digestion and stress regulation. This review may provide a theoretical reference for production strategy by regulating the digestive metabolism and homeostasis of rumen microbe through LuxS/AI-2 QS.

Key words: LuxS/AI-2 quorum sensing, biofilm, rumen microbe, community stability, feed digestion

中图分类号:

Q938.15

龙唐晖, 周江汇, 詹彦波, 张健, 赵向辉, 李艳娇, 欧阳克蕙, 邱清华. 反刍动物瘤胃微生物LuxS/AI-2群体感应研究进展[J]. 畜牧兽医学报, 2024, 55(5): 1893-1903.

LONG Tanghui, ZHOU Jianghui, ZHAN Yanbo, ZHANG Jian, ZHAO Xianghui, LI Yanjiao, OUYANG Kehui, QIU Qinghua. Research Progress on LuxS/AI-2 Quorum Sensing of Rumen Microbe in Ruminants[J]. Acta Veterinaria et Zootechnica Sinica, 2024, 55(5): 1893-1903.

参考文献

[1] MORGAVI D P,KELLY W J,JANSSEN P H,et al.Rumen microbial (meta)genomics and its application to ruminant production[J].Animal,2013,7(S1):184-201.
[2] RANAVA D,BACKES C,KARTHIKEYAN G,et al.Metabolic exchange and energetic coupling between nutritionally stressed bacterial species:role of quorum-sensing molecules[J].mBio,2021,12(1):e02758-20.
[3] MCNAB R,LAMONT R J.Microbial dinner-party conversations:the role of LuxS in interspecies communication[J].J Med Microbiol,2003,52(Pt 7):541-545.
[4] WANG Y S,BIAN Z R,WANG Y.Biofilm formation and inhibition mediated by bacterial quorum sensing[J].Appl Microbiol Biotechnol,2022,106(19):6365-6381.
[5] MITSUMORI M,XU L M,KAJIKAWA H,et al.Possible quorum sensing in the rumen microbial community:detection of quorum-sensing signal molecules from rumen bacteria[J].FEMS Microbiol Lett,2003,219(1):47-52.
[6] WON M Y,OYAMA L B,COURTNEY S J,et al.Can rumen bacteria communicate to each other?[J].Microbiome,2020,8(1):23.
[7] MILLER S T,XAVIER K B,CAMPAGNA S R,et al.Salmonella typhimurium recognizes a chemically distinct form of the bacterial quorum-sensing signal AI-2[J].Mol Cell,2004,15(5):677-687.
[8] MIRANDA V,TORCATO I M,XAVIER K B,et al.Synthesis of d-desthiobiotin-AI-2 as a novel chemical probe for autoinducer-2 quorum sensing receptors[J].Bioorg Chem,2019,92:103200.
[9] SCHAUDER S,SHOKAT K,SURETTE M G,et al.The LuxS family of bacterial autoinducers:biosynthesis of a novel quorum-sensing signal molecule[J].Mol Microbiol,2001,41(2):463-476.
[10] TORCATO I M,KASAL M R,BRITO P H,et al.Identification of novel autoinducer-2 receptors in Clostridia reveals plasticity in the binding site of the LsrB receptor family[J].J Biol Chem,2019,294(12):4450-4463.
[11] NEIDITCH M B,FEDERLE M J,MILLER S T,et al.Regulation of LuxPQ receptor activity by the quorum-sensing signal autoinducer-2[J].Mol Cell,2005,18(5):507-518.
[12] CHEN X,SCHAUDER S,POTIER N,et al.Structural identification of a bacterial quorum-sensing signal containing boron[J].Nature,2002,415(6871):545-549.
[13] RAJAMANI S,ZHU J G,PEI D H,et al.A LuxP-FRET-based reporter for the detection and quantification of AI-2 bacterial quorum-sensing signal compounds[J].Biochemistry,2007,46(13):3990-3997.
[14] LAGANENKA L,LEE J W,MALFERTHEINER L,et al.Chemotaxis and autoinducer-2 signalling mediate colonization and contribute to co-existence of Escherichia coli strains in the murine gut[J].Nat Microbiol,2023,8(2):204-217.
[15] KEIZERS M,DOBRINDT U,BERGER M.A simple biosensor-based assay for quantitative autoinducer-2 analysis[J].ACS Synth Biol,2022,11(2):747-759.
[16] KUMAR S,KUMAR C B,RAJENDRAN V,et al.Delineating virulence of Vibrio campbellii:a predominant luminescent bacterial pathogen in Indian shrimp hatcheries[J].Sci Rep,2021,11(1):15831.
[17] BISWAS S,MUKHERJEE P,MANNA T,et al.Quorum sensing autoinducer(s) and flagellum independently mediate EPS signaling in Vibrio cholerae through LuxO-independent mechanism[J].Microb Ecol,2019,77(3):616-630.
[18] TALÀ A,SIDE D D,BUCCOLIERI G,et al.Exposure to static magnetic field stimulates quorum sensing circuit in luminescent Vibrio strains of the Harveyi clade[J].PLoS One,2014,9(6):e100825.
[19] GU Y,LI B,TIAN J J,et al.The response of LuxS/AI-2 quorum sensing in Lactobacillus fermentum 2-1 to changes in environmental growth conditions[J].Ann Microbiol,2018,68(5):287-294.
[20] CHAI Y M,MA Q W,NONG X,et al.Dissecting LuxS/AI-2 quorum sensing system-mediated phenyllactic acid production mechanisms of Lactiplantibacillus plantarum L3[J].Food Res Int,2023,166:112582.
[21] AQAWI M,SIONOV R V,FRIEDMAN M,et al.The antibacterial effect of cannabigerol toward Streptococcus mutans is influenced by the autoinducers 21-CSP and AI-2[J].Biomedicines,2023,11(3):668.
[22] MENG F Q,ZHAO M W,LU Z X.The LuxS/AI-2 system regulates the probiotic activities of lactic acid bacteria[J].Trends Food Sci Technol,2022,127:272-279.
[23] HERZOG R,PESCHEK N,FRÖHLICH K S,et al.Three autoinducer molecules act in concert to control virulence gene expression in Vibrio cholerae[J].Nucleic Acids Res,2019,47(6):3171-3183.
[24] BRIDGES A A,BASSLER B L.The intragenus and interspecies quorum-sensing autoinducers exert distinct control over Vibrio cholerae biofilm formation and dispersal[J].PLoS Biol,2019,17(11):e3000429.
[25] BOYACI H,SHAH T,HURLEY A,et al.Structure,regulation,and inhibition of the quorum-sensing signal integrator LuxO[J].PLoS Biol,2016,14(5):e1002464.
[26] RAYCHAUDHURI S,JAIN V,DONGRE M.Identification of a constitutively active variant of LuxO that affects production of HA/protease and biofilm development in a non-O1,non-O139 Vibrio cholerae O110[J].Gene,2006,369:126-133.
[27] TAGA M E,MILLER S T,BASSLER B L.Lsr-mediated transport and processing of AI-2 in Salmonella typhimurium[J].Mol Microbiol,2003,50(4):1411-1427.
[28] TAGA M E,SEMMELHACK J L,BASSLER B L.The LuxS-dependent autoinducer AI-2 controls the expression of an ABC transporter that functions in AI-2 uptake in Salmonella typhimurium[J].Mol Microbiol,2001,42(3):777-793.
[29] TAGA M E,BASSLER B L.Chemical communication among bacteria[J].Proc Natl Acad Sci U S A,2003,100(S2):14549-14554.
[30] TOLKER-NIELSEN T.Biofilm development[M]//GHANNOUM M,PARSEK M,WHITELEY M,et al.Microbial Biofilms.2nd ed.Washington:American Society for Microbiology,2015:51-66.
[31] KOLTER R,GREENBERG E P.Microbial sciences:the superficial life of microbes[J].Nature,2006,441(7091):300-302.
[32] CHU P L,FENG Y M,LONG Z Q,et al.Novel benzothiazole derivatives as potential anti-quorum sensing agents for managing plant bacterial diseases:synthesis,antibacterial activity assessment,and SAR study[J].J Agric Food Chem,2023,71(17):6525-6540.
[33] RYBTKE M,HULTQVIST L D,GIVSKOV M,et al.Pseudomonas aeruginosa biofilm infections:community structure,antimicrobial tolerance and immune response[J].J Mol Biol,2015,427(23):3628-3645.
[34] HÄUSSLER S,BECKER T.The pseudomonas quinolone signal (PQS) balances life and death in Pseudomonas aeruginosa populations[J].PLoS Pathog,2008,4(9):e1000166.
[35] VENDEVILLE A,WINZER K,HEURLIER K,et al.Making ’sense’ of metabolism:autoinducer-2,LuxS and pathogenic bacteria[J].Nat Rev Microbiol,2005,3(5):383-396.
[36] WANG Y,WANG Y X,SUN L Y,et al.The LuxS/AI-2 system of Streptococcus suis[J].Appl Microbiol Biotechnol,2018,102(17):7231-7238.
[37] WANG Y,YI L,ZHANG Z C,et al.Overexpression of luxS cannot increase autoinducer-2 production,only affect the growth and biofilm formation in Streptococcus suis[J].Sci World J,2013,2013:924276.
[38] LAGANENKA L,COLIN R,SOURJIK V.Chemotaxis towards autoinducer 2 mediates autoaggregation in Escherichia coli[J].Nat Commun,2016,7(1):12984.
[39] HEGDE M,ENGLERT D L,SCHROCK S,et al.Chemotaxis to the quorum-sensing signal AI-2 requires the Tsr chemoreceptor and the periplasmic LsrB AI-2-binding protein[J].J Bacteriol,2011,193(3):768-773.
[40] WEN Y C,HUANG H M,TANG T C,et al.AI-2 represses CagA expression and bacterial adhesion,attenuating the Helicobacter pylori-induced inflammatory response of gastric epithelial cells[J].Helicobacter,2021,26(2):e12778.
[41] ANDERSON J K,HUANG J Y,WREDEN C,et al.Chemorepulsion from the quorum signal autoinducer-2 promotes Helicobacter pylori biofilm dispersal[J].mBio,2015,6(4):e00379.
[42] CLUZEL M E,ZANELLA-CLE?ON I,COZZONE A J,et al.The Staphylococcus aureus autoinducer-2 synthase LuxS is regulated by Ser/Thr phosphorylation[J].J Bacteriol,2010,192(23):6295-6301.
[43] ZHANG L J,SHEN Y,QIU L L,et al.The suppression effect of SCH-79797 on Streptococcus mutans biofilm formation[J].J Oral Microbiol,2022,14(1):2061113.
[44] SZTAJER H,LEMME A,VILCHEZ R,et al.Autoinducer-2-regulated genes in Streptococcus mutans UA159 and global metabolic effect of the luxS mutation[J].J Bacteriol,2008,190(1):401-415.
[45] RODRIGUES M V,KIS P,XAVIER K B,et al.Synthesis and potential of Autoinducer-2 and analogs to manipulate inter-species quorum sensing[J].ISR J Chem,2023,63(5-6):e202200091.
[46] MAYER C,BORGES A,FLAMENT-SIMON S C,et al.Quorum sensing architecture network in Escherichia coli virulence and pathogenesis[J].FEMS Microbiol Rev,2023,47(4):fuad031.
[47] SLATER R T,FROST L R,JOSSI S E,et al.Clostridioides difficile LuxS mediates inter-bacterial interactions within biofilms[J].Sci Rep,2019,9:9903.
[48] ARENAS J,TOMMASSEN J.Meningococcal biofilm formation:Let’s stick together[J].Trends Microbiol,2017,25(2):113-124.
[49] ROUSSEL-JAZÉDÉ V,GRIJPSTRA J,VAN DAM V,et al.Lipidation of the autotransporter NalP of Neisseria meningitidis is required for its function in the release of cell-surface-exposed proteins[J].Microbiology (Reading),2013,159(Pt 2):286-295.
[50] ROUSSEL-JAZÉDÉ V,JONGERIUS I,BOS M P,et al.NalP-mediated proteolytic release of lactoferrin-binding protein B from the meningococcal cell surface[J].Infect Immun,2010,78(7):3083-3089.
[51] VAN ULSEN P,VAN ALPHEN L,HOVE J T,et al.A Neisserial autotransporter NalP modulating the processing of other autotransporters[J].Mol Microbiol,2003,50(3):1017-1030.
[52] PENG N,CAI P,MORTIMER M,et al.The exopolysaccharide-eDNA interaction modulates 3D architecture of Bacillus subtilis biofilm[J].BMC Microbiol,2020,20:115.
[53] HOBLEY L,HARKINS C,MACPHEE C E,et al.Giving structure to the biofilm matrix:an overview of individual strategies and emerging common themes[J].FEMS Microbiol Rev,2015,39(5):649-669.
[54] GU Y,TIAN J J,ZHANG Y,et al.Dissecting signal molecule AI-2 mediated biofilm formation and environmental tolerance in Lactobacillus plantarum[J].J Biosci Bioeng,2021,131(2):153-160.
[55] MUHAMMAD M H,IDRIS A L,FAN X,et al.Beyond risk:bacterial biofilms and their regulating approaches[J].Front Microbiol,2020,11:928.
[56] KRAGH K N,HUTCHISON J B,MELAUGH G,et al.Role of multicellular aggregates in biofilm formation[J].mBio,2016,7(2):e00237.
[57] NUNAN N,WU K J,YOUNG I M,et al.Spatial distribution of bacterial communities and their relationships with the micro-architecture of soil[J].FEMS Microbiol Ecol,2003,44(2):203-215.
[58] SUGIMOTO S,OKUDA K I,MIYAKAWA R,et al.Imaging of bacterial multicellular behaviour in biofilms in liquid by atmospheric scanning electron microscopy[J].Sci Rep,2016,6:25889.
[59] LIU X Z,LIU Q M,SUN S H,et al.Exploring AI-2-mediated interspecies communications within rumen microbial communities[J].Microbiome,2022,10:167.
[60] GHALI I,SHINKAI T,MITSUMORI M.Mining of luxS genes from rumen microbial consortia by metagenomic and metatranscriptomic approaches[J].Anim Sci J,2016,87(5):666-673.
[61] XIE Y Y,SUN H Z,XUE M Y,et al.Metagenomics reveals differences in microbial composition and metabolic functions in the rumen of dairy cows with different residual feed intake[J].Anim Microbiome,2022,4(1):19.
[62] LI Q S,WANG R,MA Z Y,et al.Dietary selection of metabolically distinct microorganisms drives hydrogen metabolism in ruminants[J].ISME J,2022,16(11):2535-2546.
[63] 郭海康,万发春,沈维军,等.畜禽消化道细菌群体感应及相关调控技术研究进展[J].畜牧兽医学报,2022,53(6):1678-1688.
GUO H K,WAN F C,SHEN W J,et al.Research progress and related regulation technology on bacterial quorum sensing in the gastro-intestinal tract of livestock and poultry[J].Acta Veterinaria et Zootechnica Sinica,2022,53(6):1678-1688.(in Chinese)
[64] 冉涛,谭支良.反刍家畜瘤胃微生物群体感应[J].动物营养学报,2012,24(7):1207-1215.
RAN T,TAN Z L.Rumen microbial quorum-sensing of ruminant livestock[J].Chinese Journal of Animal Nutrition,2012,24(7):1207-1215.(in Chinese)
[65] VAHIDI M F,GHARECHAHI J,BEHMANESH M,et al.Diversity of microbes colonizing forages of varying lignocellulose properties in the sheep rumen[J].PeerJ,2021,9:e10463.
[66] COMTET-MARRE S,PARISOT N,LEPERCQ P,et al.Metatranscriptomics reveals the active bacterial and eukaryotic fibrolytic communities in the rumen of dairy cow fed a mixed diet[J].Front Microbiol,2017,8:67.
[67] MINATO H,ENDO A,OOTOMO Y,et al.Ecological treatise on the rumen fermentation:II.The amylolytic and cellulolytic activities of the fractionated bacterial portions attached to the rumen solids[J].J Gen Appl Microbiol,1966,12(1):53-69.
[68] CHENG K J,STEWART C S,DINSDALE D,et al.Electron microscopy of bacteria involved in the digestion of plant cell walls[J].Anim Feed Sci Technol,1984,10(2-3):93-120.
[69] MOSONI P,FONTY G,GOUET P.Competition between ruminal cellulolytic bacteria for adhesion to cellulose[J].Ann Zootech,1996,45(S1):298.
[70] KOIKE S,PAN J,KOBAYASHI Y,et al.Kinetics of in sacco fiber-attachment of representative ruminal cellulolytic bacteria monitored by competitive PCR[J].J Dairy Sci,2003,86(4):1429-1435.
[71] BAR-ZEEV E,BERMAN-FRANK I,GIRSHEVITZ O,et al.Revised paradigm of aquatic biofilm formation facilitated by microgel transparent exopolymer particles[J].Proc Natl Acad Sci U S A,2012,109(23):9119-9124.
[72] LENG R A.The rumen- a fermentation vat or a series of organized structured microbial consortia:implications for the mitigation of enteric methane production by feed additives[J].Livest Res Rural Dev,2011,23(12):258.
[73] SPEZIALE P,PIETROCOLA G,FOSTER T J,et al.Protein-based biofilm matrices in Staphylococci[J].Front Cell Infect Microbiol,2014,4:171.
[74] LENG R A.Interactions between microbial consortia in biofilms:a paradigm shift in rumen microbial ecology and enteric methane mitigation[J].Anim Prod Sci,2014,54(5):519-543.
[75] MCCALL A,EDGERTON M.Real-time approach to flow cell imaging of Candida albicans biofilm development[J].J Fungi,2017,3(1):13.
[76] HUWS S,MAYORGA O L,KIM E J,et al.Microbial colonization and subsequent biofilm formation by ruminal microorganisms on fresh perennial ryegrass[C]//2007 Conference on Gastrointestinal Function (CGIF).Chicago,2007.
[77] XIROS C,SHAHAB R L,STUDER M H P.A cellulolytic fungal biofilm enhances the consolidated bioconversion of cellulose to short chain fatty acids by the rumen microbiome[J].Appl Microbiol Biotechnol,2019,103(8):3355-3365.
[78] DOBRETSOV S,TEPLITSKI M,PAUL V.Mini-review:quorum sensing in the marine environment and its relationship to biofouling[J].Biofouling,2009,25(5):413-427.
[79] HUWS S A,EDWARDS J E,LIN W C,et al.Microbiomes attached to fresh perennial ryegrass are temporally resilient and adapt to changing ecological niches[J].Microbiome,2021,9(1):143.
[80] SOROKIN D Y,GUMEROV V M,RAKITIN A L,et al.Genome analysis of Chitinivibrio alkaliphilus gen.nov.,sp.nov.,a novel extremely haloalkaliphilic anaerobic chitinolytic bacterium from the candidate phylum Termite Group 3[J].Environ Microbiol,2014,16(6):1549-1565.
[81] SUEN G,WEIMER P J,STEVENSON D M,et al.The complete genome sequence of Fibrobacter succinogenes S85 reveals a cellulolytic and metabolic specialist[J].PLoS One,2011,6(4):e18814.
[82] RAHMAN N A,PARKS D H,VANWONTERGHEM I,et al.A phylogenomic analysis of the bacterial phylum Fibrobacteres[J].Front Microbiol,2016,6:1469.
[83] SHABAT S K B,SASSON G,DORON-FAIGENBOIM A,et al.Specific microbiome-dependent mechanisms underlie the energy harvest efficiency of ruminants[J].ISME J,2016,10(12):2958-2972.