Resource partitioning in relation to cohabitation of Lactobacillus species in the mouse forestomach

被引:65
作者
Tannock, Gerald W. [1 ]
Wilson, Charlotte M. [1 ]
Loach, Diane [1 ]
Cook, Gregory M. [1 ]
Eason, Jocelyn [2 ]
O'Toole, Paul W. [3 ]
Holtrop, Grietje [4 ]
Lawley, Blair [1 ]
机构
[1] Univ Otago, Dept Microbiol & Immunol, Dunedin, New Zealand
[2] Plant & Food Res, Palmerston North, New Zealand
[3] Natl Univ Ireland Univ Coll Cork, Dept Microbiol & Alimentary Pharmabiot Ctr, Cork, Ireland
[4] Univ Aberdeen, Rowett Inst Nutr & Hlth, Aberdeen, Scotland
基金
爱尔兰科学基金会;
关键词
gut; niche; adaptation; lactobacilli; resource partitioning; mathematical model; DNA-MICROARRAY DATA; ESCHERICHIA-COLI; GENE-EXPRESSION; BEHAVIOR; STRAINS; PCR;
D O I
10.1038/ismej.2011.161
中图分类号
Q14 [生态学(生物生态学)];
学科分类号
071012 ; 0713 ;
摘要
Phylogenetic analysis of gut communities of vertebrates is advanced, but the relationships, especially at the trophic level, between commensals that share gut habitats of monogastric animals have not been investigated to any extent. Lactobacillus reuteri strain 100-23 and Lactobacillus johnsonii strain 100-33 cohabit in the forestomach of mice. According to the niche exclusion principle, this should not be possible because both strains can utilise the two main fermentable carbohydrates present in the stomach digesta: glucose and maltose. We show, based on gene transcription analysis, in vitro physiological assays, and in vivo experiments that the two strains can co-exist in the forestomach habitat because 100-23 grows more rapidly using maltose, whereas 100-33 preferentially utilises glucose. Mutation of the maltose phosphorylase gene (malA) of strain 100-23 prevented its growth on maltose-containing culture medium, and resulted in the numerical dominance of 100-33 in the forestomach. The fundamental niche of L. reuteri 100-23 in the mouse forestomach can be defined in terms of 'glucose and maltose trophism'. However, its realised niche when L. johnsonii 100-33 is present is 'maltose trophism'. Hence, nutritional adaptations provide niche differentiation that assists cohabitation by the two strains through resource partitioning in the mouse forestomach. This real life, trophic phenomenon conforms to a mathematical model based on in vitro bacterial doubling times, in vitro transport rates, and concentrations of maltose and glucose in mouse stomach digesta. The ISME Journal (2012) 6, 927-938; doi:10.1038/ismej.2011.161; published online 17 November 2011
引用
收藏
页码:927 / 938
页数:12
相关论文
共 27 条
[1]  
[Anonymous], ECOLOGICAL THEATER E
[2]   Bacterial Community Variation in Human Body Habitats Across Space and Time [J].
Costello, Elizabeth K. ;
Lauber, Christian L. ;
Hamady, Micah ;
Fierer, Noah ;
Gordon, Jeffrey I. ;
Knight, Rob .
SCIENCE, 2009, 326 (5960) :1694-1697
[3]   PreP:: gene expression data pre-processing [J].
de la Nava, JG ;
van Hijum, S ;
Trelles, O .
BIOINFORMATICS, 2003, 19 (17) :2328-2329
[4]   Comparison of carbon nutrition for pathogenic and commensal Escherichia coli strains in the mouse intestine [J].
Fabich, Andrew J. ;
Jones, Shari A. ;
Chowdhury, Fatema Z. ;
Cernosek, Amanda ;
Anderson, April ;
Smalley, Darren ;
McHargue, J. Wesley ;
Hightower, G. Aaron ;
Smith, Joel T. ;
Autieri, Steven M. ;
Leatham, Mary P. ;
Lins, Jeremy J. ;
Allen, Regina L. ;
Laux, David C. ;
Cohen, Paul S. ;
Conway, Tyrrell .
INFECTION AND IMMUNITY, 2008, 76 (03) :1143-1152
[5]   Behavior of mixed populations and the problem of natural selection [J].
Gause, GF ;
Witt, AA .
AMERICAN NATURALIST, 1935, 69 :596-609
[6]   Metagenomic analysis of the human distal gut microbiome [J].
Gill, Steven R. ;
Pop, Mihai ;
DeBoy, Robert T. ;
Eckburg, Paul B. ;
Turnbaugh, Peter J. ;
Samuel, Buck S. ;
Gordon, Jeffrey I. ;
Relman, David A. ;
Fraser-Liggett, Claire M. ;
Nelson, Karen E. .
SCIENCE, 2006, 312 (5778) :1355-1359
[7]   Dissecting the genetic components of adaptation of Escherichia coli to the mouse gut [J].
Giraud, Antoine ;
Arous, Safia ;
De Paepe, Marianne ;
Gaboriau-Routhiau, Valerie ;
Bambou, Jean-Christophe ;
Rakotobe, Sabine ;
Lindner, Ariel B. ;
Taddei, Francois ;
Cerf-Bensussan, Nadine .
PLOS GENETICS, 2008, 4 (01) :0052-0061
[8]   Detection, characterization, and in vitro and in vivo expression of genes encoding S-proteins in Lactobacillus gallinarum strains isolated from chicken crops [J].
Hagen, KE ;
Guan, LL ;
Tannock, GW ;
Korver, DR ;
Allison, GE .
APPLIED AND ENVIRONMENTAL MICROBIOLOGY, 2005, 71 (11) :6633-6643
[9]  
Hammes WP., 1995, The Genera of Lactic Acid Bacteria, V2, P19
[10]   COMPETITIVE EXCLUSION PRINCIPLE [J].
HARDIN, G .
SCIENCE, 1960, 131 (3409) :1292-1297