Microbial interactions impact stress tolerance in a model oral community

被引:2
作者
Lewin, Gina R. [1 ,2 ,3 ]
Evans, Emma R. [1 ,2 ]
Whiteley, Marvin [1 ,2 ]
机构
[1] Georgia Inst Technol, Ctr Microbial Dynam & Infect, Sch Biol Sci, Atlanta, GA 30332 USA
[2] Emory Childrens Cyst Fibrosis Ctr, Atlanta, GA 30324 USA
[3] Case Western Reserve Univ, Ctr Global Hlth & Dis, Dept Pathol, Cleveland, OH 44106 USA
关键词
S; gordonii; A; actinomycetemcomitans; polymicrobial interactions; disturbance; cross-feeding; ACTINOBACILLUS-ACTINOMYCETEMCOMITANS; PORPHYROMONAS-GINGIVALIS; STREPTOCOCCUS-GORDONII; BACTERIAL DIVERSITY; RESISTANCE; VIRULENCE; IMMUNITY; SYNERGY; PLAQUE; GENES;
D O I
10.1128/spectrum.01005-24
中图分类号
Q93 [微生物学];
学科分类号
071005 ; 100705 ;
摘要
Understanding the molecular mechanisms governing microbial interactions is crucial for unraveling the complexities of microbial communities and their ecological impacts. Here, we employed a two-species model system comprising the oral bacteria Aggregatibacter actinomycetemcomitans and Streptococcus gordonii to investigate how synergistic and antagonistic interactions between microbes impact their resilience to environmental change and invasion by other microbes. We used an in vitro colony biofilm model and focused on two S. gordonii-produced extracellular molecules, L-lactate and H2O2, which are known to impact fitness of this dual-species community. While the ability of A. actinomycetemcomitans to cross-feed on S. gordonii-produced L-lactate enhanced its fitness during co-culture, this function showed little impact on the ability of co-cultures to resist environmental change. In fact, the ability of A. actinomycetemcomitans to catabolize L-lactate may be detrimental in the presence of tetracycline, highlighting the complexity of interactions under antimicrobial stress. Furthermore, H2O2, known for its antimicrobial properties, had negative impacts on both species in our model system. However, H2O2 production by S. gordonii enhanced A. actinomycetemcomitans tolerance to tetracycline, suggesting a protective role under antibiotic pressure. Finally, S. gordonii significantly inhibited the bacterium Serratia marcescens from invading in vitro biofilms, but this inhibition was lost during co-culture with A. actinomycetemcomitans and in a murine abscess model, where S. gordonii actually promoted S. marcescens invasion. These data indicate that microbial interactions can impact fitness of a bacterial community upon exposure to stresses, but these impacts are highly environment dependent.
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页数:13
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共 51 条
[1]   Cross-feeding modulates antibiotic tolerance in bacterial communities [J].
Adamowicz, Elizabeth M. ;
Flynn, Jeffrey ;
Hunter, Ryan C. ;
Harcombe, William R. .
ISME JOURNAL, 2018, 12 (11) :2723-2735
[2]   Polymicrobial Infections and Biofilms: Clinical Significance and Eradication Strategies [J].
Anju, V. T. ;
Busi, Siddhardha ;
Imchen, Madangchanok ;
Kumavath, Ranjith ;
Mohan, Mahima S. S. ;
Salim, Simi Asma ;
Subhaswaraj, Pattnaik ;
Dyavaiah, Madhu .
ANTIBIOTICS-BASEL, 2022, 11 (12)
[3]   The biogeography of infection revisited [J].
Azimi, Sheyda ;
Lewin, Gina R. ;
Whiteley, Marvin .
NATURE REVIEWS MICROBIOLOGY, 2022, 20 (10) :579-592
[4]   Developing animal models for polymicrobial diseases [J].
Bakaletz, LO .
NATURE REVIEWS MICROBIOLOGY, 2004, 2 (07) :552-568
[5]   Inter-species interactions alter antibiotic efficacy in bacterial communities [J].
Bottery, Michael J. ;
Matthews, Jessica L. ;
Wood, A. Jamie ;
Johansen, Helle Krogh ;
Pitchford, Jon W. ;
Friman, Ville-Petri .
ISME JOURNAL, 2022, 16 (03) :812-821
[6]   Ecology and evolution of antimicrobial resistance in bacterial communities [J].
Bottery, Michael J. ;
Pitchford, Jonathan W. ;
Friman, Ville-Petri .
ISME JOURNAL, 2021, 15 (04) :939-948
[7]   Endocarditis due to rare and fastidious bacteria [J].
Brouqui, P ;
Raoult, D .
CLINICAL MICROBIOLOGY REVIEWS, 2001, 14 (01) :177-+
[8]   A novel Exclusion mechanism for carbon resource partitioning in Aggregatibacter actinomycetemcomitans [J].
Brown, Stacie A. ;
Whiteley, Marvin .
JOURNAL OF BACTERIOLOGY, 2007, 189 (17) :6407-6414
[9]   Characterization of the L-Lactate Dehydrogenase from Aggregatibacter actinomycetemcomitans [J].
Brown, Stacie A. ;
Whiteley, Marvin .
PLOS ONE, 2009, 4 (11)
[10]   Host responses induced by co-infection with Porphyromonas gingivalis and Actinobacillus actinomycetemcomitans in a murine model [J].
Chen, PB ;
Davern, LB ;
Katz, J ;
Eldridge, JH ;
Michalek, SM .
ORAL MICROBIOLOGY AND IMMUNOLOGY, 1996, 11 (04) :274-281