Paenibacillus is a genus of facultative anaerobic, endospore-forming bacteria, originally included within the genus Bacillus and then reclassified as a separate genus in 1993.[8] Bacteria belonging to this genus have been detected in a variety of environments, such as: soil, water, rhizosphere, vegetable matter, forage and insect larvae, as well as clinical samples.[9][10][11][12] The name reflects: Latin paene means almost, so the paenibacilli are literally "almost bacilli". The genus includes P. larvae, which causes American foulbrood in honeybees, P. polymyxa, which is capable of fixing nitrogen, so is used in agriculture and horticulture, the Paenibacillus sp. JDR-2 which is a rich source of chemical agents for biotechnology applications, and pattern-forming strains such as P. vortex and P. dendritiformis discovered in the early 90s,[13][14][15][16][17] which develop complex colonies with intricate architectures[18][19][20][21][22] as shown in the pictures:
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A colony generated by the chiral morphotype bacteria of P. dendritiformis: The colony diameter is 5 cm and the colors indicate the bacterial density (bright yellow for high density). The branches are curly with well-defined handedness.
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A colony generated by P. vortex sp. bacteria: The colony diameter is 5 cm and the colors indicate the bacterial density (bright yellow for high density). The bright dots are the vortices described in the text.
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A colony generated by the branching (tip splitting) morphotype bacteria of P. dendritiformis: The colony diameter is 6 cm and the colors indicate the bacterial density (darker shade for higher density).
Importance
editInterest in Paenibacillus spp. has been rapidly growing since many were shown to be important[23][24][25] for agriculture and horticulture (e.g. P. polymyxa), industrial (e.g. P. amylolyticus), and medical applications (e.g. P. peoriate). These bacteria produce various extracellular enzymes such as polysaccharide-degrading enzymes and proteases, which can catalyze a wide variety of synthetic reactions in fields ranging from cosmetics to biofuel production. Various Paenibacillus spp. also produce antimicrobial substances that affect a wide spectrum of micro-organisms[26][27][28] such as fungi, soil bacteria, plant pathogenic bacteria, and even important anaerobic pathogens such as Clostridium botulinum.
More specifically, several Paenibacillus species serve as efficient plant growth-promoting rhizobacteria (PGPR), which competitively colonize plant roots and can simultaneously act as biofertilizers and as antagonists (biopesticides) of recognized root pathogens, such as bacteria, fungi, and nematodes.[29] They enhance plant growth by several direct and indirect mechanisms. Direct mechanisms include phosphate solubilization, nitrogen fixation, degradation of environmental pollutants, and hormone production. Indirect mechanisms include controlling phytopathogens by competing for resources such as iron, amino acids and sugars, as well as by producing antibiotics or lytic enzymes.[30][31] Competition for iron also serves as a strong selective force determining the microbial population in the rhizosphere. Several studies show that PGPR exert their plant growth-promoting activity by depriving native microflora of iron. Although iron is abundant in nature, the extremely low solubility of Fe3+ at pH 7 means that most organisms face the problem of obtaining enough iron from their environments. To fulfill their requirements for iron, bacteria have developed several strategies, including the reduction of ferric to ferrous ions, the secretion of high-affinity iron-chelating compounds, called siderophores, and the uptake of heterologous siderophores. P. vortex's genome, for example,[32] harbors many genes which are employed in these strategies, in particular it has the potential to produce siderophores under iron-limiting conditions.
Despite the increasing interest in Paenibacillus spp., genomic information of these bacteria is lacking. More extensive genome sequencing could provide fundamental insights into pathways involved in complex social behavior of bacteria, and can discover a source of genes with biotechnological potential.
Candidatus Paenibacillus glabratella causes white nodules and high mortality of Biomphalaria glabrata freshwater snails.[33] This is potentially important because Biomphalaria glabrata is an intermediate host of schistosomiasis.[33]
A major challenge in the dairy industry is reducing premature spoilage of fluid milk caused by microbes.[34] Paenibacillus is often isolated from both raw and pasteurized fluid milk. The most predominant Paenibacillus species isolated is Paenibacillus odorifer. Species in the Paenibacillus genus can sporulate to survive the pasteurization of milk and are subsequently able to germinate in refrigerated milk, despite the low temperatures. Many bacterial genera have a cold shock response, which involves the production of cold shock proteins that help the cell facilitate global translation recovery.[34] Little is currently known about the cold shock response in Paenibacillus compared to other species, but it has been shown that Paenibacillus species contain many genetic elements associated with the cold shock response.[35] Paenibacillus odorifer was demonstrated to carry multiple copies of these cold shock associated genetics elements.[34]
Pattern formation, self-organization, and social behaviors
editSeveral Paenibacillus species can form complex patterns on semisolid surfaces. Development of such complex colonies require self-organization and cooperative behavior of individual cells while employing sophisticated chemical communication called quorum sensing.[13][14][18][20][21][36][37][38] Pattern formation and self-organization in microbial systems is an intriguing phenomenon and reflects social behaviors of bacteria[37][39] that might provide insights into the evolutionary development of the collective action of cells in higher organisms.[13][37][40][41][42][43][44]
Pattern forming in P. vortex
editOne of the most fascinating pattern forming Paenibacillus species is P. vortex, self-lubricating, flagella-driven bacteria.[32] P. vortex organizes its colonies by generating modules, each consisting of many bacteria, which are used as building blocks for the colony as a whole. The modules are groups of bacteria that move around a common center at about 10 μm/s.
Pattern forming in P. dendritiformis
editAn additional intriguing pattern forming Paenibacillus species is P. dendritiformis, which generates two different morphotypes[13][14][18][19][20][21] – the branching (or tip-splitting) morphotype and the chiral morphotype that is marked by curly branches with well-defined handedness (see pictures).
These two pattern-forming Paenibacillus strains exhibit many distinct physiological and genetic traits, including β-galactosidase-like activity causing colonies to turn blue on X-gal plates and multiple drug resistance (MDR) (including septrin, penicillin, kanamycin, chloramphenicol, ampicillin, tetracycline, spectinomycin, streptomycin, and mitomycin C). Colonies that are grown on surfaces in Petri dishes exhibit several-fold higher drug resistance in comparison to growth in liquid media. This particular resistance is believed to be due to a surfactant-like liquid front that actually forms a particular pattern on the Petri plate.
References
edit- ^ Gao M, Yang H, Zhao J, Liu J, Sun YH, Wang YJ, Sun JG (March 2013). "Paenibacillus brassicae sp. nov., isolated from cabbage rhizosphere in Beijing, China". Antonie van Leeuwenhoek. 103 (3): 647–653. doi:10.1007/s10482-012-9849-1. PMID 23180372. S2CID 18884588.
- ^ Puri A, Padda KP, Chanway CP (October 2015). "Can a diazotrophic endophyte originally isolated from lodgepole pine colonize an agricultural crop (corn) and promote its growth?". Soil Biology and Biochemistry. 89: 210–216. doi:10.1016/j.soilbio.2015.07.012.
- ^ Puri A, Padda KP, Chanway CP (January 2016). "Evidence of nitrogen fixation and growth promotion in canola (Brassica napus L.) by an endophytic diazotroph Paenibacillus polymyxa P2b-2R". Biology and Fertility of Soils. 52 (1): 119–125. doi:10.1007/s00374-015-1051-y. S2CID 15963708.
- ^ Puri A, Padda KP, Chanway CP (June 2016). "Seedling growth promotion and nitrogen fixation by a bacterial endophyte Paenibacillus polymyxa P2b-2R and its GFP derivative in corn in a long-term trial". Symbiosis. 69 (2): 123–129. doi:10.1007/s13199-016-0385-z. S2CID 17870808.
- ^ Padda KP, Puri A, Chanway CP (April 2016). "Effect of GFP tagging of Paenibacillus polymyxa P2b-2R on its ability to promote growth of canola and tomato seedlings". Biology and Fertility of Soils. 52 (3): 377–387. doi:10.1007/s00374-015-1083-3. S2CID 18149924.
- ^ Padda KP, Puri A, Chanway CP (7 July 2016). "Plant growth promotion and nitrogen fixation in canola by an endophytic strain of Paenibacillus polymyxa and its GFP-tagged derivative in a long-term study". Botany. 94 (12): 1209–1217. doi:10.1139/cjb-2016-0075.
- ^ Yang H, Puri A, Padda KP, Chanway CP (June 2016). "Effects of Paenibacillus polymyxa inoculation and different soil nitrogen treatments on lodgepole pine seedling growth". Canadian Journal of Forest Research. 46 (6): 816–821. doi:10.1139/cjfr-2015-0456. hdl:1807/72264.
- ^ Ash C, Priest FG, Collins MD: Molecular identification of rRNA group 3 bacilli (Ash, Farrow, Wallbanks and Collins) using a PCR probe test. Proposal for the creation of a new genus Paenibacillus. Antonie van Leeuwenhoek 1993, 64:253-260.
- ^ Padda KP, Puri A, Chanway CP (2017). "Paenibacillus polymyxa: A Prominent Biofertilizer and Biocontrol Agent for Sustainable Agriculture". Agriculturally Important Microbes for Sustainable Agriculture. Springer, Singapore. pp. 165–191. doi:10.1007/978-981-10-5343-6_6. ISBN 9789811053429.
- ^ McSpadden Gardener BB (November 2004). "Ecology of Bacillus and Paenibacillus spp. in Agricultural Systems". Phytopathology. 94 (11): 1252–1258. doi:10.1094/PHYTO.2004.94.11.1252. PMID 18944463.
- ^ Montes MJ, Mercadé E, Bozal N, Guinea J (September 2004). "Paenibacillus antarcticus sp. nov., a novel psychrotolerant organism from the Antarctic environment". International Journal of Systematic and Evolutionary Microbiology. 54 (Pt 5): 1521–1526. doi:10.1099/ijs.0.63078-0. PMID 15388704.
- ^ Ouyang J, Pei Z, Lutwick L, Dalal S, Yang L, Cassai N, et al. (2008). "Case report: Paenibacillus thiaminolyticus: a new cause of human infection, inducing bacteremia in a patient on hemodialysis". Annals of Clinical and Laboratory Science. 38 (4): 393–400. PMC 2955490. PMID 18988935.
- ^ a b c d Ben-Jacob E, Cohen I (1997). "Cooperative formation of bacterial patterns.". In Shapiro JA, Dworkin M (eds.). Bacteria as Multicellular Organisms. New York: Oxford University Press. pp. 394–416.
- ^ a b c Ben-Jacob E, Cohen I, Gutnick DL (1998). "Cooperative organization of bacterial colonies: from genotype to morphotype". Annual Review of Microbiology. 52: 779–806. doi:10.1146/annurev.micro.52.1.779. PMID 9891813.
- ^ Ben-Jacob E, Schochet O, Tenenbaum A, Cohen I, Czirók A, Vicsek T (March 1994). "Generic modelling of cooperative growth patterns in bacterial colonies". Nature. 368 (6466): 46–9. Bibcode:1994Natur.368...46B. doi:10.1038/368046a0. PMID 8107881. S2CID 3054995.
- ^ Ben-Jacob E, Shmueli H, Shochet O, Tenenbaum A (September 1992). "Adaptive self-organization during growth of bacterial colonies". Physica A: Statistical Mechanics and Its Applications. 187 (3–4): 378–424. Bibcode:1992PhyA..187..378B. doi:10.1016/0378-4371(92)90002-8.
- ^ Ben-Jacob E, Shochet O, Tenenbaum A, Avidan O (1995). "Evolution of complexity during growth of bacterial colonies.". In Cladis PE, Palffy-Muhorey P (eds.). NATO Advanced Research Workshop; Santa Fe, USA. Addison-Wesley Publishing Company. pp. 619–633.
- ^ a b c Ben-Jacob E (June 2003). "Bacterial self-organization: co-enhancement of complexification and adaptability in a dynamic environment". Philosophical Transactions. Series A, Mathematical, Physical, and Engineering Sciences. 361 (1807): 1283–312. Bibcode:2003RSPTA.361.1283B. doi:10.1098/rsta.2003.1199. PMID 12816612. S2CID 5213232.
- ^ a b Ben-Jacob E, Cohen I, Golding I, Gutnick DL, Tcherpakov M, Helbing D, Ron IG (July 2000). "Bacterial cooperative organization under antibiotic stress". Physica A: Statistical Mechanics and Its Applications. 282 (1–2): 247–82. Bibcode:2000PhyA..282..247B. doi:10.1016/S0378-4371(00)00093-5.
- ^ a b c Ben-Jacob E, Cohen I, Levine H (June 2000). "Cooperative self-organization of microorganisms". Advances in Physics. 49 (4): 395–554. Bibcode:2000AdPhy..49..395B. doi:10.1080/000187300405228. S2CID 121881941.
- ^ a b c Ben-Jacob E, Levine H (February 2006). "Self-engineering capabilities of bacteria". Journal of the Royal Society, Interface. 3 (6): 197–214. doi:10.1098/rsif.2005.0089. PMC 1618491. PMID 16849231.
- ^ Ingham CJ, Ben Jacob E (February 2008). "Swarming and complex pattern formation in Paenibacillus vortex studied by imaging and tracking cells". BMC Microbiology. 8: 36. doi:10.1186/1471-2180-8-36. PMC 2268691. PMID 18298829.
- ^ Choi KK, Park CW, Kim SY, Lyoo WS, Lee SH, Lee JW (2004). "Polyvinyl alcohol degradation by Microbacterium barkeri KCCM 10507 and Paeniblacillus amylolyticus KCCM 10508 in dyeing wastewater". Journal of Microbiology and Biotechnology. 14: 1009–1013.
- ^ Konishi J, Maruhashi K (September 2003). "2-(2'-Hydroxyphenyl)benzene sulfinate desulfinase from the thermophilic desulfurizing bacterium Paenibacillus sp. strain A11-2: purification and characterization". Applied Microbiology and Biotechnology. 62 (4): 356–61. doi:10.1007/s00253-003-1331-6. PMID 12743754. S2CID 7956236.
- ^ Nielsen P, Sørensen J (March 1997). "Multi-target and medium-independent fungal antagonism by hydrolytic enzymes in Paenibacillus polymyxa and Bacillus pumilus strains from barley rhizosphere". FEMS Microbiology Ecology. 22 (3): 183–192. doi:10.1111/j.1574-6941.1997.tb00370.x.
- ^ Girardin H, Albagnac C, Dargaignaratz C, Nguyen-The C, Carlin F (May 2002). "Antimicrobial activity of foodborne Paenibacillus and Bacillus spp. against Clostridium botulinum". Journal of Food Protection. 65 (5): 806–13. doi:10.4315/0362-028x-65.5.806. PMID 12030292.
- ^ Piuri M, Sanchez-Rivas C, Ruzal SM (July 1998). "A novel antimicrobial activity of a Paenibacillus polymyxa strain isolated from regional fermented sausages". Letters in Applied Microbiology. 27 (1): 9–13. doi:10.1046/j.1472-765x.1998.00374.x. hdl:20.500.12110/paper_02668254_v27_n1_p9_Piuri. PMID 9722991. S2CID 34127618.
- ^ von der Weid I, Alviano DS, Santos AL, Soares RM, Alviano CS, Seldin L (2003). "Antimicrobial activity of Paenibacillus peoriae strain NRRL BD-62 against a broad spectrum of phytopathogenic bacteria and fungi". Journal of Applied Microbiology. 95 (5): 1143–51. doi:10.1046/j.1365-2672.2003.02097.x. PMID 14633044. S2CID 22884479.
- ^ Bloemberg GV, Lugtenberg BJ (August 2001). "Molecular basis of plant growth promotion and biocontrol by rhizobacteria". Current Opinion in Plant Biology. 4 (4): 343–50. doi:10.1016/s1369-5266(00)00183-7. PMID 11418345.
- ^ Kloepper JW, Leong J, Teintze M, Schroth MN (August 1980). "Enhanced plant growth by siderophores produced by plant growth-promoting rhizobacteria". Nature. 286 (5776): 885–886. Bibcode:1980Natur.286..885K. doi:10.1038/286885a0. S2CID 40761689.
- ^ Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, Paré PW, Kloepper JW (April 2003). "Bacterial volatiles promote growth in Arabidopsis". Proceedings of the National Academy of Sciences of the United States of America. 100 (8): 4927–4932. Bibcode:2003PNAS..100.4927R. doi:10.1073/pnas.0730845100. PMC 153657. PMID 12684534.
- ^ a b Sirota-Madi A, Olender T, Helman Y, Ingham C, Brainis I, Roth D, et al. (December 2010). "Genome sequence of the pattern forming Paenibacillus vortex bacterium reveals potential for thriving in complex environments". BMC Genomics. 11: 710. doi:10.1186/1471-2164-11-710. PMC 3012674. PMID 21167037.
- ^ a b Duval D, Galinier R, Mouahid G, Toulza E, Allienne JF, Portela J, et al. (February 2015). "A novel bacterial pathogen of Biomphalaria glabrata: a potential weapon for schistosomiasis control?". PLOS Neglected Tropical Diseases. 9 (2): e0003489. doi:10.1371/journal.pntd.0003489. PMC 4342248. PMID 25719489.
- ^ a b c Beno SM, Cheng RA, Orsi RH, Duncan DR, Guo X, Kovac J, et al. (January 2020). Marco ML (ed.). "Paenibacillus odorifer, the Predominant Paenibacillus Species Isolated from Milk in the United States, Demonstrates Genetic and Phenotypic Conservation of Psychrotolerance but Clade-Associated Differences in Nitrogen Metabolic Pathways". mSphere. 5 (1). doi:10.1128/mSphere.00739-19. PMC 7407005. PMID 31969477.
- ^ Moreno Switt AI, Andrus AD, Ranieri ML, Orsi RH, Ivy R, den Bakker HC, et al. (January 2014). "Genomic comparison of sporeforming bacilli isolated from milk". BMC Genomics. 15 (1): 26. doi:10.1186/1471-2164-15-26. PMC 3902026. PMID 24422886.
- ^ Bassler BL, Losick R (April 2006). "Bacterially speaking". Cell. 125 (2): 237–46. doi:10.1016/j.cell.2006.04.001. PMID 16630813. S2CID 17056045.
- ^ a b c Ben Jacob E, Becker I, Shapira Y, Levine H (August 2004). "Bacterial linguistic communication and social intelligence". Trends in Microbiology. 12 (8): 366–372. doi:10.1016/j.tim.2004.06.006. PMID 15276612.
- ^ Dunny GM, Brickman TJ, Dworkin M (April 2008). "Multicellular behavior in bacteria: communication, cooperation, competition and cheating". BioEssays. 30 (4): 296–8. doi:10.1002/bies.20740. PMID 18348154.
- ^ Galperin MY, Gomelsky M (2005). "Bacterial Signal Transduction Modules: from Genomics to Biology". ASM News. 71: 326–333.
- ^ Aguilar C, Vlamakis H, Losick R, Kolter R (December 2007). "Thinking about Bacillus subtilis as a multicellular organism". Current Opinion in Microbiology. 10 (6): 638–643. doi:10.1016/j.mib.2007.09.006. PMC 2174258. PMID 17977783.
- ^ Dwyer DJ, Kohanski MA, Collins JJ (December 2008). "Networking opportunities for bacteria". Cell. 135 (7): 1153–6. doi:10.1016/j.cell.2008.12.016. PMC 2728295. PMID 19109881.
- ^ Kolter R, Greenberg EP (May 2006). "Microbial sciences: the superficial life of microbes". Nature. 441 (7091): 300–2. Bibcode:2006Natur.441..300K. doi:10.1038/441300a. PMID 16710410. S2CID 4430171.
- ^ Shapiro JA (1998). "Thinking about bacterial populations as multicellular organisms". Annual Review of Microbiology. 52: 81–104. doi:10.1146/annurev.micro.52.1.81. PMID 9891794.
- ^ Shapiro JA, Dworkin M (1997). Bacteria as multicellular organisms (1st ed.). USA: Oxford University Press.
Further reading
edit- Sirota-Madi A, Olender T, Helman Y, Ingham C, Brainis I, Roth D, et al. (December 2010). "Genome sequence of the pattern forming Paenibacillus vortex bacterium reveals potential for thriving in complex environments". BMC Genomics. 11: 710. doi:10.1186/1471-2164-11-710. PMC 3012674. PMID 21167037.
- da Mota FF, Gomes EA, Paiva E, Seldin L (July 2005). "Assessment of the diversity of Paenibacillus species in environmental samples by a novel rpoB-based PCR-DGGE method". FEMS Microbiology Ecology. 53 (2): 317–28. doi:10.1016/j.femsec.2005.01.017. PMID 16329951. S2CID 22545561.
- da Mota FF, Gomes EA, Paiva E, Rosado AS, Seldin L (2004). "Use of rpoB gene analysis for identification of nitrogen-fixing Paenibacillus species as an alternative to the 16S rRNA gene". Letters in Applied Microbiology. 39 (1): 34–40. doi:10.1111/j.1472-765X.2004.01536.x. PMID 15189285. S2CID 20682334.
External links
edit- "Paenibacillus Taxonomy". LPSN - List of Prokaryotic names with Standing in Nomenclature.
- "Paenibacillus". Bac Dive - the Bacterial Diversity Metadatabase.
- Prof. Eshel Ben-Jacob home page