Cell morphology drives spatial patterning in microbial communities

Proceedings of the National Academy of Sciences of the United States of America

Volumn 114, Issue 3, 2017, Pages E280-E286

  Smith, William P J ^a   Davit, Yohan ^b   Osborne, James M ^c   Kim, Wook D ^a,d   Foster, Kevin R ^a   Pitt Francis, Joe M ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITÉ PAUL SABATIER   (France)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d DUQUESNE UNIVERSITY   (United States)

Author keywords

Biofilms; Biophysics; Cell morphology; Self organization; Synthetic biology

Indexed keywords

AMINO ACID; MREB PROTEIN; ESCHERICHIA COLI PROTEIN; MREB PROTEIN, E COLI;

BACTERIAL CELL; BACTERIUM COLONY; BIOFILM; CELL LINEAGE; CELL SHAPE; CELL STRUCTURE; CONFERENCE PAPER; CONFOCAL LASER SCANNING MICROSCOPY; CONTROLLED STUDY; ESCHERICHIA COLI; EXPERIMENTAL TEST; IMAGE SEGMENTATION; MICROBIAL COMMUNITY; NONHUMAN; NUTRIENT AVAILABILITY; NUTRIENT SUPPLY; PRIORITY JOURNAL; RETINA ROD; STAPHYLOCOCCUS AUREUS; BIOENGINEERING; BIOLOGICAL MODEL; BIOPHYSICS; COMPUTER SIMULATION; CYTOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; MICROBIAL CONSORTIUM; MUTATION; PHENOTYPE; PHYSIOLOGY; SYNTHETIC BIOLOGY;

BIOENGINEERING; BIOFILMS; BIOPHYSICAL PHENOMENA; COMPUTER SIMULATION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MICROBIAL CONSORTIA; MODELS, BIOLOGICAL; MUTATION; PHENOTYPE; SYNTHETIC BIOLOGY;

EID: 85009728711     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1613007114     Document Type: Article

References (58)

1. Starr MP, Skerman VBD (1965) Bacterial diversity: The natural history of selected morphologically unusual bacteria. Annu Rev Microbiol 19:407-454.
2. Vos P, et al. (2011) Bergey's Manual of Systematic Bacteriology: The Firmicutes (Springer Science & Business Media, Dordrecht, The Netherlands), Vol 3.
3. Cabeen MT, Jacobs-Wagner C (2005) Bacterial cell shape. Nat Rev Microbiol 3(8): 601-610.
4. Siefert JL, Fox GE (1998) Phylogenetic mapping of bacterial morphology. Microbiology 144 (Pt 10):2803-2808.
5. Tamames J, Gonzalez-Moreno M, Mingorance J, Valencia A, Vicente M (2001) Bringing gene order into bacterial shape. Trends Genet 17(3):124-126.
6. Kysela DT, Randich AM, Caccamo PD, Brun YV (2016) Diversity takes shape: Understanding the mechanistic and adaptive basis of bacterial morphology. PLoS Biol 14(10):e1002565.
7. Young KD (2006) The selective value of bacterial shape. Microbiol Mol Biol Rev 70(3):660-703.
8. Justice SS, Hunstad Da, Cegelski L, Hultgren SJ (2008) Morphological plasticity as a bacterial survival strategy. Nat Rev Microbiol 6(2):162-168.
9. Young KD (2004) Bacterial shape. Mol Microbiol 49(3):571-580.
10. Young KD (2007) Bacterial morphology: Why have different shapes? Curr Opin Microbiol 10(6):596-600.
11. Young KD (2010) Bacterial shape: Two-dimensional questions and possibilities. Annu Rev Microbiol 64:223-240.
12. Nakamura S, Adachi Y, Goto T, Magariyama Y (2006) Improvement in motion efficiency of the spirochete Brachyspira pilosicoli in viscous environments. Biophys J 90(8):3019-3026.
13. McLoughlin K, Schluter J, Rakoff-Nahoum S, Smith AL, Foster KR (2016) Host selection of microbiota via differential adhesion. Cell Host Microbe 19(4):550-559.
14. Coyte KZ, Schluter J, Foster KR (2015) The ecology of the microbiome: Networks, competition, and stability. Science 350(6261):663-666.
15. Wolcott RD, Ehrlich GD (2008) Biofilms and chronic infections. JAMA 299(22): 2682-2684.
16. Stewart PS, Costerton JW (2001) Antibiotic resistance of bacteria in biofilms. Lancet 358(9276):135-138.
17. Klapper I, Dockery J (2010) Mathematical description of microbial biofilms. SIAM Rev 52(2):221-265.
18. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM (1995) Microbial biofilms. Annu Rev Microbiol 49:711-745.
19. Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: From the natural environment to infectious diseases. Nat Rev Microbiol 2(2):95-108.
20. Volfson D, Cookson S, Hasty J, Tsimring LS (2008) Biomechanical ordering of dense cell populations. Proc Natl Acad Sci USA 105(40):15346-15351.
21. Boyer D, et al. (2011) Buckling instability in ordered bacterial colonies. Phys Biol 8(2):026008.
22. Cho H, et al. (2007) Self-organization in high-density bacterial colonies: Efficient crowd control. PLoS Biol 5(11):e302.
23. Copeland MF, Weibel DB (2009) Bacterial swarming: A model system for studying dynamic self-assembly. Soft Matter 5(6):1174-1187.
24. Rudge TJ, Federici F, Steiner PJ, Kan A, Haseloff J (2013) Cell polarity-driven instability generates self-organized, fractal patterning of cell layers. ACS Synth Biol 2(12): 705-714.
25. Ghosh P, Mondal J, Ben-Jacob E, Levine H (2015) Mechanically-driven phase separation in a growing bacterial colony. Proc Natl Acad Sci USA 112(17):E2166-E2173.
26. Picioreanu C, van Loosdrecht MCM, Heijnen JJ (1998) Mathematical modeling of biofilm structure with a hybrid differential-discrete cellular automaton approach. Biotechnol Bioeng 58(1):101-116.
27. Kreft J-U (2004) Biofilms promote altruism. Microbiology 150(Pt 8):2751-2760.
28. Nadell CD, Foster KR, Xavier JB (2010) Emergence of spatial structure in cell groups and the evolution of cooperation. PLoS Comput Biol 6(3):e1000716.
29. Schluter J, Foster KR (2012) The evolution of mutualism in gut microbiota via host epithelial selection. PLoS Biol 10(11):e1001424.
30. Nadell CD, et al. (2013) Cutting through the complexity of cell collectives. Proc Biol Sci 280(1755):20122770.
31. Estrela S, Brown SP (2013) Metabolic and demographic feedbacks shape the emergent spatial structure and function of microbial communities. PLoS Comput Biol 9(12):e1003398.
32. Storck T, Picioreanu C, Virdis B, Batstone DJ (2014) Variable cell morphology approach for individual-based modeling of microbial communities. Biophys J 106(9): 2037-2048.
33. Nakayama M, Shigemune N, Tsugukuni T, Tokuda H, Miyamoto T (2011) Difference of EGCg adhesion on cell surface between Staphylococcus aureus and Escherichia coli visualized by electron microscopy after novel indirect staining with cerium chloride. J Microbiol Methods 86(1):97-103.
34. Matthew J, Arduino JC (2007) Staphylococcus aureus SEM (image 6486). Accessed July 7, 2016.
35. Rocky Mountain Laboratories, NIAID, NIH (2006) Escherichia coli SEM. Accessed July 7, 2016.
36. Christensen BB, Haagensen JAJ, Heydorn AJ, Molin S (2002) Metabolic commensalism and competition in a two-species microbial consortium. Appl Environ Microbiol 68(5):2495-2502.
37. Hansen SK, Rainey PB, Haagensen JAJ, Molin S (2007) Evolution of species interactions in a biofilm community. Nature 445(7127):533-536.
38. Elias S, Banin E (2012) Multi-species biofilms: living with friendly neighbors. FEMS Microbiol Rev 36(5):990-1004.
39. Wimpenny J, Manz W, Szewzyk U (2000) Heterogeneity in biofilms. FEMS Microbiol Rev 24(5):661-671.
40. Nadell CD, Xavier JB, Foster KR (2009) The sociobiology of biofilms. FEMS Microbiol Rev 33(1):206-224.
41. Kim W, Racimo F, Schluter J, Levy SB, Foster KR (2014) Importance of positioning for microbial evolution. Proc Natl Acad Sci USA 111(16):E1639-E16347.
42. Picioreanu C, Van Loosdrecht MCM, Heijnen JJ (2000) Effect of diffusive and convective substrate transport on biofilm structure formation: a two-dimensional modeling study. Biotechnol Bioeng 69(5):504-515.
43. Kreft JU, Wimpenny JWT (2001) Effect of EPS on biofilm structure and function as revealed by an individual-based model of biofilm growth. Water Sci Technol 43(6):135-141.
44. Monds RD, et al. (2014) Systematic perturbation of cytoskeletal function reveals a linear scaling relationship between cell geometry and fitness. Cell Rep 9(4): 1528-1537.
45. Nava GM, Friedrichsen HJ, Stappenbeck TS (2011) Spatial organization of intestinal microbiota in the mouse ascending colon. ISME J 5(4):627-638.
46. Serra DO, Richter AM, Klauck G, Mika F, Hengge R (2013) Microanatomy at cellular resolution and spatial order of physiological differentiation in a bacterial biofilm. MBio 4(2):e00103-e00113.
47. Bergkessel M, Basta DW, Newman DK (2016) The physiology of growth arrest: Uniting molecular and environmental microbiology. Nat Rev Microbiol 14(9):549-562.
48. Hendrickx L, Hausner M, Wuertz S (2003) Natural genetic transformation in monoculture Acinetobacter sp. strain BD413 biofilms. Appl Environ Microbiol 69(3):1721-1727.
49. Picioreanu C, et al. (2007) Microbial motility involvement in biofilm structure formation - a 3D modelling study. Water Sci Technol 55(8-9):337-343.
50. Xavier JB, Foster KR (2007) Cooperation and conflict in microbial biofilms. Proc Natl Acad Sci USA 104(3):876-881.
51. Heisenberg CP, Belläiche Y (2013) Forces in tissue morphogenesis and patterning. Cell 153(5):948-962.
52. Basan M, Elgeti J, Hannezo E, RappelW-J, Levine H (2013) Alignment of cellular motility forces with tissue flow as a mechanism for efficient wound healing. Proc Natl Acad Sci USA 110(7):2452-2459.
53. Sekiguchi Y, Kamagata Y, Nakamura K, Ohashi A, Harada H (1999) Fluorescence in situ hybridization using 16S rRNA-targeted oligonucleotides reveals localization of methanogens and selected uncultured bacteria in mesophilic and thermophilic sludge granules. Appl Environ Microbiol 65(3):1280-1288.
54. Wilmes P, et al. (2009) Natural acidophilic biofilm communities reflect distinct organismal and functional organization. ISME J 3(2):266-270.
55. Brenner K, Arnold FH (2011) Self-organization, layered structure, and aggregation enhance persistence of a synthetic biofilm consortium. PLoS One 6(2):e16791.
56. Lenski RE, Rose MR, Simpson SC, Tadler SC (2016) Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2, 000 generations. Am Nat 138(6):1315-1341.
57. Kim W, Levy SB, Foster KR (2016) Rapid radiation in bacteria leads to a division of labour. Nat Commun 7:10508.
58. Otsu N (1975) A threshold selection method from gray-level histograms. Automatica 11(285-296):23-27.