Microbial mutualism dynamics governed by dose-dependent toxicity of cross-fed nutrients

ISME Journal

Volumn 11, Issue 2, 2017, Pages 337-348

  La Sarre, Breah ^a   McCully, Alexandra L ^a   Lennon, Jay T ^a   McKinlay, James B ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANOXIC CONDITIONS; BACTERIUM; BIOTRANSFORMATION; COEXISTENCE; DOSE-RESPONSE RELATIONSHIP; ECOSYSTEM DYNAMICS; ENERGY FLOW; EXPERIMENTAL STUDY; GENETIC ENGINEERING; METABOLISM; MICROBIAL ACTIVITY; MUTUALISM; NUTRIENT DYNAMICS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; RHODOPSEUDOMONAS PALUSTRIS;

CARBON; CARBOXYLIC ACID; NITROGEN;

BIOLOGICAL MODEL; ECOSYSTEM; ESCHERICHIA COLI; FERMENTATION; GENETICS; HETEROTROPHY; METABOLISM; PATHOGENICITY; PHYSIOLOGY; RHODOPSEUDOMONAS; SYMBIOSIS;

CARBON; CARBOXYLIC ACIDS; ECOSYSTEM; ESCHERICHIA COLI; FERMENTATION; HETEROTROPHIC PROCESSES; MODELS, BIOLOGICAL; NITROGEN; RHODOPSEUDOMONAS; SYMBIOSIS;

EID: 85000461226     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2016.141     Document Type: Article

References (55)

1. Abbott BJ. (1973). Ethanol inhibition of a bacterium (Acinetobacter calcoaceticus) in chemostat culture. J Gen Microbiol 75: 383-389.
2. Adam B, Klawonn I, Svedén JB, Bergkvist J, Nahar N, Walve J, et al. (2016). N2-fixation, ammonium release and N-Transfer to the microbial and classical food web within a plankton community. ISME J 10: 450-459.
3. Alvarez LA, Exton DA, Timmis KN, Suggett DJ, McGenity TJ. (2009). Characterization of marine isoprene-degrading communities. Environ Microbiol 11: 3280-3291.
4. Barney BM, Eberhart LJ, Ohlert JM, Knutson CM, Plunkett MH. (2015). Gene deletions resulting in increased nitrogen release by Azotobacter vinelandii: Application of a novel nitrogen biosensor. Appl Environ Microbiol 81: 4316-4328.
5. Barnhill AE, Weeks KE, Xiong N, Day TA, Carlson SA. (2010). Identification of multiresistant Salmonella isolates capable of subsisting on antibiotics. Appl Environ Microbiol 76: 2678-2680.
6. Ding J, Liu BF, Ren NQ, Xing DF, Guo WQ, Xu JF, et al. (2009). Hydrogen production from glucose by co-culture of Clostridium butyricum and immobilized Rhodopseudomonas faecalis RLD-53. Int J Hydrogen Energy 34: 3647-3652.
7. Ducret A, Quardokus E, Brun Y. (2016). MicrobeJ, a high throughput tool for quantitative bacterial cell detection and analysis. Nat Microbiol 1: 16077.
8. Estrela S, Trisos CH, Brown SP. (2012). From metabolism to ecology: cross-feeding interactions shape the balance between polymicrobial conflict and mutualism. Am Nat 180: 566-576.
9. Fang HHP, Zhu H, Zhang T. (2006). Phototrophic hydrogen production from glucose by pure and co-cultures of Clostridium butyricum and Rhodobacter sphaeroides. Int J Hydrogen Energy 31: 2223-2230.
10. Fuhrman JA. (2009). Microbial community structure and its functional implications. Nature 459: 193-199.
11. Geddes BA, Ryu M-H, Mus F, Garcia Costas A, Peters JW, Voigt CA, et al. (2015). Use of plant colonizing bacteria as chassis for transfer of N2-fixation to cereals. Curr Opin Biotechnol 32: 216-222.
12. Harcombe W. (2010). Novel cooperation experimentally evolved between species. Evolution 64: 2166-2172.
13. Hillesland KL, Stahl DA. (2010). Rapid evolution of stability and productivity at the origin of a microbial mutualism. Proc Natl Acad Sci USA 107: 2124-2129.
14. Hom EFY, Murray AW. (2014). Niche engineering demonstrates a latent capacity for fungal-Algal mutualism. Science 345: 94-88.
15. Huang CB, Alimova Y, Myers TM, Ebersole JL. (2011). Short-And medium-chain fatty acids exhibit antimicrobial activity for oral microorganisms. Arch Oral Biol 56: 650-654.
16. Huang JJ, Heiniger EK, McKinlay JB, Harwood CS. (2010). Production of hydrogen gas from light and the inorganic electron donor thiosulfate by Rhodopseudomonas palustris. Appl Environ Microbiol 76: 7717-7722.
17. Jiao Y, Navid A, Stewart BJ, McKinlay JB, Thelen MP, Pett-Ridge J. (2012). Syntrophic metabolism of a co-culture containing Clostridium cellulolyticum and Rhodopseudomonas palustris for hydrogen production. Int J Hydrogen Energy 37: 11719-11726.
18. Johns NI, Blazejewski T, Gomes AL, Wang HH. (2016). Principles for designing synthetic microbial communities. Curr Opin Microbiol 31: 146-153.
19. Kim HJ, Boedicker JQ, Choi JW, Ismagilov RF. (2008). Defined spatial structure stabilizes a synthetic multispecies bacterial community. Proc Natl Acad Sci USA 105: 18188-18193.
20. Kim M, Harwood CS. (1991). Regulation of benzoate-CoA ligase in Rhodopseudomonas palustris. FEMS Micrbiol Lett 83: 199-203.
21. Klitgord N, Segrè D. (2010). Environments that induce synthetic microbial ecosystems. PLoS Comput Biol 6: e1001002.
22. Kremer TA, LaSarre B, Posto AL, McKinlay JB. (2015). N2 gas is an effective fertilizer for bioethanol production by Zymomonas mobilis. Proc Natl Acad Sci USA 112: 2222-2226.
23. Kunz DA, Nagappan O, Silva-Avalos J, Delong GT. (1992). Utilization of cyanide as nitrogenous substrate by Pseudomonas fluorescens NCIMB 11764: evidence for multiple pathways of metabolic conversion. Appl Environ Microbiol 58: 2022-2029.
24. Larimer FW, Chain P, Hauser L, Lamerdin J, Malfatti S, Do L, et al. (2004). Complete genome sequence of the metabolically versatile photosynthetic bacterium Rhodopseudomonas palustris. Nat Biotechnol 22: 55-61.
25. Lee IH, Fredrickson AG, Tsuchiya HM. (1976). Dynamics of mixed cultures of Lactobacillus plantarum and Propionibacterium shermanii. Biotechnol Bioeng 18: 513-526.
26. Lindemann SR, Bernstein HC, Song H-S, Fredrickson JK, Fields MW, Shou W, et al. (2016). Engineering microbial consortia for controllable outputs. ISME J 10: 2077-2084.
27. Louis P, Scott KP, Duncan SH, Flint HJ. (2007). Understanding the effects of diet on bacterial metabolism in the large intestine. J Appl Microbiol 102: 1197-1208.
28. McInerney MJ, Sieber JR, Gunsalus RP. (2009). Syntrophy in anaerobic global carbon cycles. Curr Opin Biotechnol 20: 623-632.
29. McKinlay JB, Harwood CS. (2011). Calvin cycle flux, pathway constraints, and substrate oxidation state together determine the H2 biofuel yield in photoheterotrophic bacteria. mBio 2: e00323-10.
30. McKinlay JB, Harwood CS. (2010). Carbon dioxide fixation as a central redox cofactor recycling mechanism in bacteria. Proc Natl Acad Sci USA 107: 11669-11675.
31. McKinlay JB, Zeikus JG, Vieille C. (2005). Insights into Actinobacillus succinogenes fermentative metabolism in a chemically defined growth medium. Appl Environ Microbiol 71: 6651-6656.
32. Mee MT, Collins JJ, Church GM, Wang HH. (2014). Syntrophic exchange in synthetic microbial communities. Proc Natl Acad Sci USA 111: E2149-E2156.
33. Meyer JS, Tsuchiya HM, Fredrickson AG. (1975). Dynamics of mixed populations having complementary metabolism. Biotechnol Bioeng 17: 1065-1081.
34. Momeni B, Chen C-C, Hillesland KL, Waite A, Shou W. (2011). Using artificial systems to explore the ecology and evolution of symbioses. Cell Mol Life Sci 68: 1353-1368.
35. Morris BEL, Henneberger R, Huber H, Moissl-Eichinger C. (2013). Microbial syntrophy: interaction for the common good. FEMS Microbiol Rev 37: 384-406.
36. Morris JJ. (2015). Black Queen evolution: the role of leakiness in structuring microbial communities. Trends Genet 31: 475-482.
37. Morris JJ Lenski RE, Zinser ER. (2012). The Black Queen Hypothesis: evolution of dependencies through adaptive gene loss. mBio 3: e00036-12.
38. Oda Y, Slagman S-J, Meijer WG, Forney LJ, Gottschal JC. (2000). Influence of growth rate and starvation on fluorescent in situ hybridization of Rhodopseudomonas palustris. FEMS Microbiol Ecol 32: 205-213.
39. Odom JM, Wall JD. (1983). Photoproduction of H2 from cellulose by an anaerobic bacterial coculture. Appl Environ Microbiol 45: 1300-1305.
40. Ortiz-Marquez JCF, Do Nascimento M, Dublan M de LA, Curatti L. (2012). Association with an ammoniumexcreting bacterium allows diazotrophic culture of oilrich eukaryotic microalgae. Appl Environ Microbiol 78: 2345-2352.
41. Pelletier DA, Hurst GB, Foote LJ, Lankford PK, McKeown CK, Lu TY, et al. (2008). A general system for studying protein-protein interactions in Gram-negative bacteria. J Proteome Res 7: 3319-3328.
42. Rey FE, Oda Y, Harwood CS. (2006). Regulation of uptake hydrogenase and effects of hydrogen utilization on gene expression in Rhodopseudomonas palustris. J Bacteriol 188: 6143-6152.
43. Russell JB, Diez-Gonzalez F. (1997). The Effects of fermentation acids on bacterial growth. Adv Microb Physiol 39: 205-234.
44. Sachs JL, Mueller UG, Wilcox TP, Bull JJ. (2004). The evolution of cooperation. Q Rev Biol 79: 135-160.
45. Schink B. (2002). Synergistic interactions in the microbial world. Antonie Van Leeuwenhoek 81: 257-261.
46. Shou W, Ram S, Vilar JMG. (2007). Synthetic cooperation in engineered yeast populations. Proc Natl Acad Sci USA 104: 1877-1882.
47. Sousa DZ, Smidt H, Alves MM, Stams AJM. (2009). Ecophysiology of syntrophic communities that degrade saturated and unsaturated long-chain fatty acids. FEMS Microbiol Ecol 68: 257-272.
48. Summers ZM, Fogarty HE, Leang C, Franks AE, Malvankar NS, Lovley DR. (2010). Direct exchange of electrons within aggregates of an evolved syntrophic coculture of anaerobic bacteria. Science 330: 1413-1415.
49. Sun Q, Xiao W, Xi D, Shi JP, Yan X, Zhou ZH. (2010). Statistical optimization of biohydrogen production from sucrose by a co-culture of Clostridium acidisoli and Rhodobacter sphaeroides. Int J Hydrogen Energy 35: 4076-4084.
50. Wanner U, Egli T. (1990). Dynamics of microbial growth and cell composition in batch culture. FEMS Microbiol Lett 75: 19-43.
51. Widder S, Allen RJ, Pfeiffer T, Curtis TP, Wiuf C, Sloan WT, et al. (2016). Challenges in microbial ecology: building predictive understanding of community function and dynamics. ISME J 10.1038/ismej.2016.45.
52. Yakunin AF, Hallenbeck PC. (2002). AmtB is necessary for NH4 +-induced nitrogenase switch-off and ADPribosylation in Rhodobacter capsulatus. J Bacteriol 184: 4081-4088.
53. Zelezniak A, Andrejev S, Ponomarova O, Mende DR, Bork P, Patil KR. (2015). Metabolic dependencies drive species co-occurrence in diverse microbial communities. Proc Natl Acad Sci USA 112: 6449-6454.
54. Zhang T, Yan Y, He S, Ping S, Alam KM, Han Y, et al. (2012). Involvement of the ammonium transporter AmtB in nitrogenase regulation and ammonium excretion in Pseudomonas stutzeri A1501. Res Microbiol 163: 332-339.
55. Zomorrodi AR, Segrè D. (2015). Synthetic ecology of microbes: mathematical models and applications. J Mol Biol 428: 837-861.