Paenibacillus

Paenibacillus
Scientific classification
Kingdom: Bacteria
Division: Firmicutes
Class: Bacilli
Order: Bacillales
Family: Paenibacillaceae
Genus: Paenibacillus
Ash et al. 1994
Species

P. agarexedens
P. agaridevorans
P. alginolyticus
P. alkaliterrae
P. alvei
P. amylolyticus
P. anaericanus
P. antarcticus
P. assamensis
P. azoreducens
P. azotofixans
P. barcinonensis
P. borealis
P. brasilensis
P. brassicae[1]
P. campinasensis
P. chinjuensis
P. chitinolyticus
P. chondroitinus
P. cineris
P. cookii
P. curdlanolyticus
P. daejeonensis
P. dendritiformis
P. durum
P. ehimensis
P. elgii
P. favisporus
P. glucanolyticus
P. glycanilyticus
P. gordonae
P. graminis
P. granivorans
P. hodogayensis
P. illinoisensis
P. jamilae
P. kobensis
P. koleovorans
P. koreensis
P. kribbensis
P. lactis
P. larvae
P. lautus
P. lentimorbus
P. macerans
P. macquariensis
P. massiliensis
P. mendelii
P. motobuensis
P. naphthalenovorans
P. nematophilus
P. odorifer
P. pabuli
P. peoriae
P. phoenicis
P. phyllosphaerae
P. polymyxa[2][3]
P. popilliae
P. pulvifaciens
P. rhizosphaerae
P. sanguinis
P. stellifer
P. terrae
P. thiaminolyticus
P. timonensis
P. tylopili
P. turicensis
P. validus
P. vortex
P. vulneris
P. wynnii
P. xylanilyticus

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.[4] 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.[5][6][7][8] The name reflects: Latin paene means almost, so the paenibacilli are literally "almost bacilli. The genus includes P. larvae, which is known to cause American foulbrood in honeybees, the P. polymyxa, which is capable of fixing nitrogen, so is used in agriculture and horticulture, the Paenibacillus sp. JDR-2 which is known to be 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,[9][10][11][12][13] which are known to develop complex colonies with intricate architectures[14][15][16][17][18] as is illustrated in the pictures.

Importance

Interest in Paenibacillus spp. has been a rapidly growing since many were shown to be important[19][20][21] 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[22][23][24] 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.[25] 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.[26][27] 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,[28] 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 is causing white nodules and high mortalities of Biomphalaria glabrata freshwater snails.[29] This is potentially important because Biomphalaria glabrata is an intermediate host transmitting schistosomiasis.[29]

Pattern formation, self-organization, and social behaviors

Several 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.[9][10][14][16][17][30][31][32] Pattern formation and self-organization in microbial systems is an intriguing phenomenon and reflects social behaviors of bacteria[31][33] that might provide insights into the evolutionary development of the collective action of cells in higher organisms.[9][31][34][35][36][37][38]

Pattern forming in P. vortex

One of the most fascinating pattern forming Paenibacillus species is P. vortex, self-lubricating, flagella-driven bacteria.[28] 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

An additional intriguing pattern forming Paenibacillus species is P. dendritiformis, which is known to be able to generate two different morphotypes[9][10][14][15][16][17] – 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

  1. ↑ Gao, Miao; Yang, Hui; Zhao, Ji; Liu, Jun; Sun, Yan-hua; Wang, Yu-jiong; Sun, Jian-guang (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.
  2. ↑ Puri, Akshit; Padda, Kiran Preet; Chanway, Chris P (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.
  3. ↑ Puri, Akshit; Padda, Kiran Preet; Chanway, Chris P (August 25, 2015). "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. doi:10.1007/s00374-015-1051-y.
  4. ↑ 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.
  5. ↑ Lal S, Tabacchioni S: Ecology and biotechnological potential of Paenibacillus polymyxa: a minireview. Indian J Microbiol 2009, 49:2-10.
  6. ↑ McSpadden Gardener BB: Ecology of Bacillus and Paenibacillus spp. in Agricultural Systems. Phytopathology 2004, 94:1252-1258.
  7. ↑ Montes MJ, Mercade E, Bozal N, Guinea J: Paenibacillus antarcticus sp. nov., a novel psychrotolerant organism from the Antarctic environment. Int J Syst Evol Microbiol 2004, 54:1521-1526.
  8. ↑ Ouyang J, Pei Z, Lutwick L, Dalal S, Yang L, Cassai N, Sandhu K, Hanna B, Wieczorek RL, Bluth M, Pincus MR: Case report: Paenibacillus thiaminolyticus: a new cause of human infection, inducing bacteremia in a patient on hemodialysis. Ann Clin Lab Sci 2008, 38:393-400.
  9. 1 2 3 4 Ben-Jacob E, Cohen I: Cooperative formation of bacterial patterns. In Bacteria as Multicellular Organisms Edited by Shapiro JA, Dworkin M. New York: Oxford University Press; 1997: 394-416
  10. 1 2 3 Ben-Jacob E, Cohen I, Gutnick DL: Cooperative organization of bacterial colonies: from genotype to morphotype. Annu Rev Microbiol 1998, 52:779-806.
  11. ↑ Ben-Jacob E, Schochet O, Tenenbaum A, Cohen I, Czirok A, Vicsek T: Generic modelling of cooperative growth patterns in bacterial colonies. Nature 1994, 368:46-49.
  12. ↑ Ben-Jacob E, Shmueli H, Shochet O, Tenenbaum A: Adaptive self-organization during growth of bacterial colonies. Physica A 1992, 187:378-424.
  13. ↑ Ben-Jacob E, Shochet O, Tenenbaum A, Avidan O: Evolution of complexity during growth of bacterial colonies. In NATO Advanced Research Workshop; Santa Fe, USA. Edited by Cladis PE, Palffy-Muhorey P. Addison-Wesley Publishing Company; 1995: 619-633.
  14. 1 2 3 Ben-Jacob E: Bacterial self-organization: co-enhancement of complexification and adaptability in a dynamic environment. Phil Trans R Soc Lond A 2003, 361:1283-1312.
  15. 1 2 Ben-Jacob E, Cohen I, Golding I, Gutnick DL, Tcherpakov M, Helbing D, Ron IG: Bacterial cooperative organization under antibiotic stress. Physica A 2000, 282:247-282.
  16. 1 2 3 Ben-Jacob E, Cohen I, Levine H: Cooperative self-organization of microorganisms. Adv Phys 2000, 49:395-554.
  17. 1 2 3 Ben-Jacob E, Levine H: Self-engineering capabilities of bacteria. J R Soc Interface 2005, 3:197-214.
  18. ↑ Ingham CJ, Ben-Jacob E: Swarming and complex pattern formation in Paenibacillus vortex studied by imaging and tracking cells. BMC Microbiol 2008, 8:36.
  19. ↑ Choi KK, Park CW, Kim SY, Lyoo WS, Lee SH, Lee JW: Polyvinyl alcohol degradation by Microbacterium barkeri KCCM 10507 and Paeniblacillus amylolyticus KCCM 10508 in dyeing wastewater. J Microbiol Biotechnol 2004, 14:1009-1013.
  20. ↑ Konishi J, Maruhashi K: 2-(2'-Hydroxyphenyl)benzene sulfinate desulfinase from the thermophilic desulfurizing bacterium Paenibacillus sp. strain A11-2: purification and characterization. Appl Microbiol Biotechnol 2003, 62:356-361.
  21. ↑ Nielsen P, Sorensen J: Multi-target and medium-independent fungal antagonism by hydrolytic enzymes in Paenibacillus polymyxa and Bacillus pumilus strains from barley rhizosphere. Fems Microbiol Ecol 1997, 22:183-192.
  22. ↑ Girardin H, Albagnac C, Dargaignaratz C, Nguyen-The C, Carlin F: Antimicrobial activity of foodborne Paenibacillus and Bacillus spp. against Clostridium botulinum. J Food Prot 2002, 65:806-813.
  23. ↑ Piuri M, Sanchez-Rivas C, Ruzal SM: A novel antimicrobial activity of a Paenibacillus polymyxa strain isolated from regional fermented sausages. Lett Appl Microbiol 1998, 27:9-13.
  24. ↑ von der Weid I, Alviano DS, Santos AL, Soares RM, Alviano CS, Seldin L: Antimicrobial activity of Paenibacillus peoriae strain NRRL BD-62 against a broad spectrum of phytopathogenic bacteria and fungi. J Appl Microbiol 2003, 95:1143-1151.
  25. ↑ Bloemberg GV, Lugtenberg BJ: Molecular basis of plant growth promotion and biocontrol by rhizobacteria. Curr Opin Plant Biol 2001, 4:343-350.
  26. ↑ Kloepper JW, Leong J, Teintze M, Schroth MN: Enhanced plant growth by siderophores produced by plant growth-promoting rhizobacteria. Nature 1980, 286:885-886.
  27. ↑ Ryu CM, Farag MA, Hu CH, Reddy MS, Wei HX, Pare PW, Kloepper JW: Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci U S A 2003, 100:4927-4932.
  28. 1 2 Sirota-Madi A, Olender T, Helman Y, Ingham C, Brainis I, Roth D, Hagi E, Brodsky L, Leshkowitz D, Galatenko V, et al: Genome sequence of the pattern forming Paenibacillus vortex bacterium reveals potential for thriving in complex environments. BMC Genomics, 11:710.
  29. 1 2 Duval D., Galinier R., Mouahid G., Toulza E., Allienne J. F., et al. (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.
  30. ↑ Bassler BL, Losick R: Bacterially speaking. Cell 2006, 125:237-246.
  31. 1 2 3 Ben-Jacob E, Becker I, Shapira Y, Levine H: Bacterial linguistic communication and social intelligence. Trends Microbiol 2004, 12:366-372.
  32. ↑ Dunny GM, Brickman TJ, Dworkin M: Multicellular behavior in bacteria: communication, cooperation, competition and cheating. Bioessays 2008, 30:296-298.
  33. ↑ Galperin MY, Gomelsky M: Bacterial Signal Transduction Modules: from Genomics to Biology. ASM News 2005, 71:326-333.
  34. ↑ Aguilar C, Vlamakis H, Losick R, Kolter R: Thinking about Bacillus subtilis as a multicellular organism. Curr Opin Microbiol 2007, 10:638-643.
  35. ↑ Dwyer DJ, Kohanski MA, Collins JJ: Networking opportunities for bacteria. Cell 2008, 135:1153-1156.
  36. ↑ Kolter R, Greenberg EP: Microbial sciences: the superficial life of microbes. Nature 2006, 441:300-302.
  37. ↑ Shapiro JA: Thinking about bacterial populations as multicellular organisms. Annu Rev Microbiol 1998, 52:81-104.
  38. ↑ Shapiro JA, Dworkin M: Bacteria as multicellular organisms. 1st edn: Oxford University Press, USA; 1997.

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