Changes in the genetic requirements for microbial interactions with increasing community complexity

eLife

Volumn 7, Issue , 2018, Pages

  Morin, Manon ^a   Pierce, Emily C ^a   Dutton, Rachel J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; MESSENGER RNA;

AMINO ACID SYNTHESIS; ARTICLE; BACTERIAL GROWTH; BIOFILM; CELL GROWTH ASSAY; CHEESE; COLONY FORMING UNIT; COMMUNITY STRUCTURE; DNA EXTRACTION; DNA FRAGMENTATION; DOWN REGULATION; ENERGY METABOLISM; ENERGY YIELD; ESCHERICHIA COLI; GENE EXPRESSION; GENE TRANSFER; GEOTRICHUM CANDIDUM; GROWTH CURVE; HAFNIA ALVEI; METABOLISM; MICROBIAL COMMUNITY; NONHUMAN; ORGANISMAL INTERACTION; OXIDATIVE STRESS; PENICILLIUM CAMEMBERTI; POLYMERASE CHAIN REACTION; PSEUDOMONAS PSYCHROPHILA; SIGNAL TRANSDUCTION; STRESS; TRANSCRIPTION REGULATION; TRANSPOSON; UPREGULATION; WHOLE GENOME SEQUENCING; DNA BARCODING; ECOSYSTEM; GENETICS; HIGH THROUGHPUT SEQUENCING; MICROFLORA;

DNA BARCODING, TAXONOMIC; DNA TRANSPOSABLE ELEMENTS; ECOSYSTEM; ESCHERICHIA COLI; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MICROBIAL INTERACTIONS; MICROBIOTA;

EID: 85054454705     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.37072     Document Type: Article

References (58)

1. Albar AH, Almehdar HA, Uversky VN, Redwan EM. 2014. Structural heterogeneity and multifunctionality of lactoferrin. Current Protein & Peptide Science 15:778–797. DOI: https://doi.org/10.2174/1389203715666140919124530, PMID: 25245670
2. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the keio collection. Molecular Systems Biology 2:2006.0008. DOI: https://doi.org/10.1038/msb4100050, PMID: 16738554
3. Belenguer A, Duncan SH, Calder AG, Holtrop G, Louis P, Lobley GE, Flint HJ. 2006. Two routes of metabolic cross-feeding between Bifidobacterium adolescentis and butyrate-producing anaerobes from the human gut. Applied and Environmental Microbiology 72:3593–3599. DOI: https://doi.org/10.1128/AEM.72.5.3593-3599. 2006, PMID: 16672507
4. Billick I, Case TJ. 1994. Higher order interactions in ecological communities: what are they and how can they be detected? Ecology 75:1529–1543. DOI: https://doi.org/10.2307/1939614
5. Boutrou R, Aziza M, Amrane A. 2006b. Enhanced proteolytic activities of Geotrichum candidum and Penicillium camembertii in mixed culture. Enzyme and Microbial Technology 39:325–331. DOI: https://doi.org/10.1016/j. enzmictec.2005.11.003
6. Boutrou R, Guéguen M. 2005. Interests in Geotrichum candidum for cheese technology. International Journal of Food Microbiology 102:1–20. DOI: https://doi.org/10.1016/j.ijfoodmicro.2004.12.028, PMID: 15924999
7. Boutrou R, Kerriou L, Gassi J-Y. 2006a. Contribution of Geotrichum candidum to the proteolysis of soft cheese. International Dairy Journal 16:775–783. DOI: https://doi.org/10.1016/j.idairyj.2005.07.007
8. Cashel M, Rudd KE. 1996. The Stringent Response. In: Neidhart FC, Ingraham JL, Brooks L. K, Magasanik B, Schaechter M, Edwin U. H (Eds). Escherichia coli and Salmonella; Cellular and Molecular Biology 2. American Society for Microbiology. p. 1410–1438.
9. Chorianopoulos NG, Giaouris ED, Kourkoutas Y, Nychas GJ. 2010. Inhibition of the early stage of Salmonella enterica serovar Enteritidis biofilm development on stainless steel by cell-free supernatant of a Hafnia alvei culture. Applied and Environmental Microbiology 76:2018–2022. DOI: https://doi.org/10.1128/AEM.02093-09, PMID: 20097823
10. Coia JE, Johnston Y, Steers NJ, Hanson MF. 2001. A survey of the prevalence of Escherichia coli O157 in raw meats, raw cow’s milk and raw-milk cheeses in south-east Scotland. International Journal of Food Microbiology 66:63–69. DOI: https://doi.org/10.1016/S0168-1605(00)00490-6, PMID: 11407549
11. Croucher NJ, Thomson NR. 2010. Studying bacterial transcriptomes using RNA-seq. Current Opinion in Microbiology 13:619–624. DOI: https://doi.org/10.1016/j.mib.2010.09.009, PMID: 20888288
12. De Vuyst L, Leroy F. 2011. Cross-feeding between bifidobacteria and butyrate-producing colon bacteria explains bifdobacterial competitiveness, butyrate production, and gas production. International Journal of Food Microbiology 149:73–80. DOI: https://doi.org/10.1016/j.ijfoodmicro.2011.03.003, PMID: 21450362
13. Dieuleveux V, Van Der Pyl D, Chataud J, Gueguen M. 1998. Purification and characterization of anti-Listeria compounds produced by Geotrichum candidum. Applied and Environmental Microbiology 64:800–803. PMID: 9464426
14. Dorel C, Lejeune P, Rodrigue A. 2006. The Cpx system of Escherichia coli, a strategic signaling pathway for confronting adverse conditions and for settling biofilm communities? Research in Microbiology 157:306–314. DOI: https://doi.org/10.1016/j.resmic.2005.12.003, PMID: 16487683
15. Falkowski PG, Fenchel T, Delong EF. 2008. The microbial engines that drive Earth’s biogeochemical cycles. Science 320:1034–1039. DOI: https://doi.org/10.1126/science.1153213, PMID: 18497287
16. Faust K, Raes J. 2012. Microbial interactions: from networks to models. Nature Reviews Microbiology 10:538– 550. DOI: https://doi.org/10.1038/nrmicro2832, PMID: 22796884
17. Flint HJ, Scott KP, Louis P, Duncan SH. 2012. The role of the gut microbiota in nutrition and health. Nature Reviews Gastroenterology & Hepatology 9:577–589. DOI: https://doi.org/10.1038/nrgastro.2012.156, PMID: 22 945443
18. Frank JF, Marth EH, Olson NF. 1977. Survival of Enteropathogenic and Non-Pathogenic Escherichia coli During the Manufacture of Camembert Cheese. Journal of Food Protection 40:835–842. DOI: https://doi.org/10.4315/0362-028X-40.12.835
19. Freilich S, Zarecki R, Eilam O, Segal ES, Henry CS, Kupiec M, Gophna U, Sharan R, Ruppin E. 2011. Competitive and cooperative metabolic interactions in bacterial communities. Nature Communications 2:589. DOI: https://doi.org/10.1038/ncomms1597, PMID: 22158444
20. Friedman J, Higgins LM, Gore J. 2017. Community structure follows simple assembly rules in microbial microcosms. Nature Ecology & Evolution 1:109. DOI: https://doi.org/10.1038/s41559-017-0109, PMID: 288126 87
21. Galia W, Leriche F, Cruveiller S, Garnier C, Navratil V, Dubost A, Blanquet-Diot S, Thevenot-Sergentet D. 2017. Strand-specific transcriptomes of Enterohemorrhagic Escherichia coli in response to interactions with ground beef microbiota: interactions between microorganisms in raw meat. BMC Genomics 18:574. DOI: https://doi. org/10.1186/s12864-017-3957-2, PMID: 28774270
22. Gambino M, Cappitelli F. 2016. Mini-review: Biofilm responses to oxidative stress. Biofouling 32:167–178. DOI: https://doi.org/10.1080/08927014.2015.1134515, PMID: 26901587
23. Ghrist AC, Heil G, Stauffer GV. 2001. GcvR interacts with GcvA to inhibit activation of the Escherichia coli glycine cleavage operon. Microbiology 147:2215–2221. DOI: https://doi.org/10.1099/00221287-147-8-2215, PMID: 11495998
24. Ghrist AC, Stauffer GV. 1995. Characterization of the Escherichia coli gcvR gene encoding a negative regulator of gcv expression. Journal of Bacteriology 177:4980–4984. DOI: https://doi.org/10.1128/jb.177.17.4980-4984. 1995, PMID: 7665475
25. Goldford JE, Lu N, Bajić D, Estrela S, Tikhonov M, Sanchez-Gorostiaga A, Segrè D, Mehta P, Sanchez A. 2018. Emergent simplicity in microbial community assembly. Science 361:469–474. DOI: https://doi.org/10.1126/science.aat1168, PMID: 30072533
26. Goodman AL, McNulty NP, Zhao Y, Leip D, Mitra RD, Lozupone CA, Knight R, Gordon JI. 2009. Identifying genetic determinants needed to establish a human gut symbiont in its habitat. Cell Host & Microbe 6:279–289. DOI: https://doi.org/10.1016/j.chom.2009.08.003, PMID: 19748469
27. Grenier F, Matteau D, Baby V, Rodrigue S. 2014. Complete genome sequence of Escherichia coli BW25113. Genome Announcements 2. DOI: https://doi.org/10.1128/genomeA.01038-14, PMID: 25323716
28. Guinee TP. 2004. Salting and the role of salt in cheese. International Journal of Dairy Technology 57:99–109. DOI: https://doi.org/10.1111/j.1471-0307.2004.00145.x
29. Gunsalus RP. 1992. Control of electron flow in Escherichia coli: coordinated transcription of respiratory pathway genes. Journal of Bacteriology 174:7069–7074. DOI: https://doi.org/10.1128/jb.174.22.7069-7074.1992, PMID: 1331024
30. Hallatschek O, Hersen P, Ramanathan S, Nelson DR. 2007. Genetic drift at expanding frontiers promotes gene segregation. PNAS 104:19926–19930. DOI: https://doi.org/10.1073/pnas.0710150104, PMID: 18056799
31. Hider RC, Kong X. 2010. Chemistry and biology of siderophores. Natural Product Reports 27:637–657. DOI: https://doi.org/10.1039/b906679a, PMID: 20376388
32. Kanehisa M, Sato Y, Morishima K. 2016. BlastKOALA and GhostKOALA: KEGG Tools for Functional Characterization of Genome and Metagenome Sequences. Journal of Molecular Biology 428:726–731. DOI: https://doi.org/10.1016/j.jmb.2015.11.006, PMID: 26585406
33. Kastman EK, Kamelamela N, Norville JW, Cosetta CM, Dutton RJ, Wolfe BE. 2016. Biotic Interactions Shape the Ecological Distributions of Staphylococcus Species. mBio 7. DOI: https://doi.org/10.1128/mBio.01157-16, PMID: 27795388
34. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A. 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. DOI: https://doi.org/10.1093/bioinformatics/bts199, PMID: 22543367
35. Koren S, Walenz BP, Berlin K, Miller JR, Bergman NH, Phillippy AM. 2017. Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Research 27:722–736. DOI: https://doi. org/10.1101/gr.215087.116, PMID: 28298431
36. Landini P. 2009. Cross-talk mechanisms in biofilm formation and responses to environmental and physiological stress in Escherichia coli. Research in Microbiology 160:259–266. DOI: https://doi.org/10.1016/j.resmic.2009. 03.001, PMID: 19345733
37. Lawrence M, Huber W, Pagès H, Aboyoun P, Carlson M, Gentleman R, Morgan MT, Carey VJ. 2013. Software for computing and annotating genomic ranges. PLoS Computational Biology 9:e1003118. DOI: https://doi.org/10.1371/journal.pcbi.1003118, PMID: 23950696
38. Love MI, Anders S, Kim V, Huber W. 2015. RNA-Seq workflow: gene-level exploratory analysis and differential expression. F1000Research 4:1070. DOI: https://doi.org/10.12688/f1000research.7035.1, PMID: 26674615
39. Markowitz VM, Chen IM, Palaniappan K, Chu K, Szeto E, Grechkin Y, Ratner A, Jacob B, Huang J, Williams P, Huntemann M, Anderson I, Mavromatis K, Ivanova NN, Kyrpides NC. 2012. IMG: the Integrated Microbial Genomes database and comparative analysis system. Nucleic Acids Research 40:D115–D122. DOI: https://doi. org/10.1093/nar/gkr1044, PMID: 22194640
40. McAdam PR, Richardson EJ, Fitzgerald JR. 2014. High-throughput sequencing for the study of bacterial pathogen biology. Current Opinion in Microbiology 19:106–113. DOI: https://doi.org/10.1016/j.mib.2014.06. 002, PMID: 25033019
41. Momeni B, Xie L, Shou W. 2017. Lotka-Volterra pairwise modeling fails to capture diverse pairwise microbial interactions. eLife 6:e25051. DOI: https://doi.org/10.7554/eLife.25051, PMID: 28350295
42. Monnet C, Back A, Irlinger F. 2012. Growth of aerobic ripening bacteria at the cheese surface is limited by the availability of iron. Applied and Environmental Microbiology 78:3185–3192. DOI: https://doi.org/10.1128/AEM. 00085-12, PMID: 22367081
43. Montet MP, Jamet E, Ganet S, Dizin M, Miszczycha S, Dunière L, Thevenot D, Vernozy-Rozand C. 2009. Growth and survival of Acid-Resistant and Non-Acid-Resistant Shiga-Toxin-Producing Escherichia coli strains during the manufacture and ripening of camembert cheese. International Journal of Microbiology 2009:1–10. DOI: https://doi.org/10.1155/2009/653481, PMID: 20016668
44. Olson MA, Siebach TW, Griffitts JS, Wilson E, Erickson DL. 2018. Genome-Wide identification of fitness factors in Mastitis-Associated Escherichia coli. Applied and Environmental Microbiology 84. DOI: https://doi.org/10. 1128/AEM.02190-17, PMID: 29101196
45. Pacheco AR, Moel M, Segre D. 2018. Costless metabolic secretions as drivers of interspecies interactions in microbial ecosystems. bioRxiv. DOI: https://doi.org/10.1101/300046
46. Price MN, Wetmore KM, Waters RJ, Callaghan M, Ray J, Liu H, Kuehl JV, Melnyk RA, Lamson JS, Suh Y, Carlson HK, Esquivel Z, Sadeeshkumar H, Chakraborty R, Zane GM, Rubin BE, Wall JD, Visel A, Bristow J, Blow MJ, et al. 2018. Mutant phenotypes for thousands of bacterial genes of unknown function. Nature 557:503–509. DOI: https://doi.org/10.1038/s41586-018-0124-0, PMID: 29769716
47. Raymond KN, Dertz EA, Kim SS. 2003. Enterobactin: an archetype for microbial iron transport. PNAS 100:3584– 3588. DOI: https://doi.org/10.1073/pnas.0630018100, PMID: 12655062
48. Sanchez-Gorostiaga A, Bajić D, Osborne ML, Poyatos JF, Sanchez A. 2018. Deep annotation of protein function across diverse. bioRxiv. DOI: https://doi.org/10.1101/333534
49. Sezonov G, Joseleau-Petit D, D’Ari R. 2007. Escherichia coli physiology in Luria-Bertani broth. Journal of Bacteriology 189:8746–8749. DOI: https://doi.org/10.1128/JB.01368-07, PMID: 17905994
50. Stubbendieck RM, Straight PD. 2016. Multifaceted Interfaces of Bacterial Competition. Journal of Bacteriology 198:2145–2155. DOI: https://doi.org/10.1128/JB.00275-16, PMID: 27246570
51. Traxler MF, Seyedsayamdost MR, Clardy J, Kolter R. 2012. Interspecies modulation of bacterial development through iron competition and siderophore piracy. Molecular Microbiology 86:628–644. DOI: https://doi.org/10. 1111/mmi.12008, PMID: 22931126
52. Trmčić A, Chauhan K, Kent DJ, Ralyea RD, Martin NH, Boor KJ, Wiedmann M. 2016. Coliform detection in cheese is associated with specific cheese characteristics, but no association was found with pathogen detection. Journal of Dairy Science 99:6105–6120. DOI: https://doi.org/10.3168/jds.2016-11112, PMID: 272 89158
53. van Opijnen T, Camilli A. 2013. Transposon insertion sequencing: a new tool for systems-level analysis of microorganisms. Nature Reviews Microbiology 11:435–442. DOI: https://doi.org/10.1038/nrmicro3033, PMID: 23712350
54. Wackwitz B, Bongaerts J, Goodman SD, Unden G. 1999. Growth phase-dependent regulation of nuoA-N expression in Escherichia coli K-12 by the Fis protein: upstream binding sites and bioenergetic significance. Molecular and General Genetics MGG 262:876–883. DOI: https://doi.org/10.1007/s004380051153, PMID: 1062 8873
55. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S, Cuomo CA, Zeng Q, Wortman J, Young SK, Earl AM. 2014. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 9:e112963. DOI: https://doi.org/10.1371/journal.pone.0112963, PMID: 25409509
56. Wetmore KM, Price MN, Waters RJ, Lamson JS, He J, Hoover CA, Blow MJ, Bristow J, Butland G, Arkin AP, Deutschbauer A. 2015. Rapid quantification of mutant fitness in diverse Bacteria by sequencing randomly bar-coded transposons. mBio 6:e00306-15. DOI: https://doi.org/10.1128/mBio.00306-15, PMID: 25968644
57. Wolfe BE, Button JE, Santarelli M, Dutton RJ. 2014. Cheese rind communities provide tractable systems for in situ and in vitro studies of microbial diversity. Cell 158:422–433. DOI: https://doi.org/10.1016/j.cell.2014.05. 041, PMID: 25036636
58. Yu G, Wang LG, Han Y, He QY. 2012. clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS: A Journal of Integrative Biology 16:284–287. DOI: https://doi.org/10.1089/omi.2011.0118, PMID: 22455463