Table 5.

Experimental evidences showing influence of filamentous phage on competitiveness of host bacteria

Influence on host bacterial competitiveness	Filamentous phage – host bacterium	Changes in host phenotype	Reference
Phages in theory of bacterial adaptation: As an agent to improve adaptation of bacterial host toward abiotic stresses
Increase in tolerance to high temperature (35°C)	Xf2 – X. campestrispv. Oryzae N5850	• Altered growth pattern (a slow growth in first 60 hr followed by fast growth)	Kamiunten and Wakimoto (1981)
Development of adaptive phenotype due to reduction in rate of cell division and growth rate	M13 – E. coli S‐26	• Reduction in growth rate due to increase in mean generation time (25%) and duration of lag phase	Brown and Dowell (1968)
	φRSM (φRSM3, φRSM4) – R. solanacearum (MAFF730139, MAFF106611, UW551 )	• Reduction in growth rate by ~60%	Askora, Kawasaki, Usami, Fujie, and Yamada (2009)
	φRSS1, φRSM1 – R. solanacearum C319; Ps29		Yamada et al. (2007)
	φM13 – E. coli W6		Wan and Goddard (2012)
	φM13‐km – E. coli TOP10F	• Reduction in growth rate	Lin et al. (2011)
	M13 – E. coli HfrC		Roy & Mitra (1970)
	f327 – Pseudoalteromonas sp. BSi20327		Yu et al. (2015)
	M13 – Escherichia coli 112‐12		Salivar, Tzagoloff, and Pratt (1964)
	Cf1c – X. campestris pv. Citri		Kuo, Tan, Su, and Yang (1991)
Tolerant to radiation	φRSS1, φRSM1 – R. solanacearum C319; Ps29	• Increase dark coloration and pigmentation	Yamada et al. (2007)
	φRSM (φRSM3, φRSM4) – R. solanacearum (MAFF730139, MAFF106611 UW551 )		Askora et al. (2009)
Regulation of host bacterial community under seasonal fluctuation in extreme arctic environment	f327 – Pseudoalteromonas sp. BSi20327	• Reduction in cell density and tolerance to NaCl and H2O2 coupled with increase in motility and chemotaxis (escape from nutrient‐deficient, highly saline environments during arctic winter; and avoid over blooming under H2O2, nutrient and radiation abundance of arctic summer)	Yu et al. (2015)
Development of freeze‐fracture resistance	fd – E. coli HB11	• Increased total lipid content (25%) of outer membrane without affecting relative concentration of phospholipids	Bayer and Bayer (1986)
Provide adaptive fitness to ensure survival in limited‐energy deep sea environment	SW1 – Shewanella piezotolerans WP3	• Reduction in swarming motility due to decreased production of lateral flagella with concomitant increase in number of filamentous phages	Jian, Xiao, and Wang (2013)
Increase in adaptation to tolerate and sequester high levels of copper and other heavy metals	Unknown – Ralstonia pickettii strains (12D and 12J)	• Horizontal transfer of metal resistance and transporter genes, and zot‐like toxin	Yang et al. (2010)
Increase in tolerance to alkaline pH and salt stress; maintenance of redox and energy state	f1 – E. coli	• Induction of phage shock protein response (secretion of pIV secretin); maintenance of PMF‐ and ATP‐dependent protein secretion	Joly et al. (2010)
Tolerant to desiccation	Pf – P. aeruginosa	• Increased cellular viscosity, aggregation, and adhesion; promotion of liquid crystalline organization of biofilm matrix	Secor et al. (2015)
Generation of high cellular energy during early growth phase; reduction in survival during acid shock	M13 – E. coli	• Upregulation of phosphotransferase; downregulation of acid stress and stationary phase transition genes; impairment of oxidative and acid‐resistance systems	Karlsson, Malmborg‐Hager, Albrekt, and Borrebaeck (2005)
Phages in theory of microbial competition: As an agent to protect the bacterial inoculant from allelopathy effect
Development of tolerance to multiple colicins (E1, E2, and E3)	f1 – E. coli K38	• Increase in deoxycholate sensitivity, leakage of b‐lactamase, and number of defective F‐pili	Boeke, Model, and Zinder (1982)
	f1 – E. coli GM1, JM1	• Modifications in tolA and tolB colicin transporter	Sun and Webster (1986)
Provide heteroimmunity	CTXφ – V. cholerae	• Divergence of phage repressors and their cognate operators (rstR‐ig‐2)	Kimsey and Waldor (1998)
Provide homoimmunity	YpfΦ – Y. pestis biovar Orientalis (CO92), Antiqua (IP550‐HC1), Medievalis (IP1865–12))	• Stable integration of YpfΦ genome as multiple tandem repeats into host chromosome providing homoimmunity to phages	Chouikha et al. (2010)
Phage in theories of microbial colonization and antagonism: As an agent to ensure better colonization of host bacteria and control bacterial pathogens
Increase in colonization potential to new surfaces by increase virulence, transmissibility, infect wide host range, toxin production, biofilm and aggregation	Nf or MDA – Neisseria meningitidis Z2491	Prevalence (90%) of hyper invasive pathogenic strains Development of virulence due to transfer of meningococcal disease associated (MDA) pathogenicity island and zonula occludens toxin (zot)‐like protein	Bille et al. (2005), Joseph et al. (2011)
	Pf4 – P. aeruginosa PAO1	Increase in virulence and evolution of super infective form; enhanced stability of biofilms Triggering of biofilm formation with small size hollow colony formation	Rice et al. (2009)
	CTXφ – Vibrio cholerae O395	Development of virulent cholera causing strain Acquiring of ability to produce cholera toxin ctxAB	Waldor and Mekalanos (1996)
	Xf2 – X. campestris pv. Oryzae N5850	Increase in virulence (larger size lesions) Increase in EPS production	Kamiunten and Wakimoto (1981)
	Ypfφ – Yersinia pestis biovar Orientalis	Emergence of highly competitive, virulent (low LD50) plague causing new pathogen with epidemic spread Increase in toxin production, stability of Ypfφ integration in bacterial host chromosome, secretion of phages having ability to infect new hosts; horizontal transfer of toxin genes	Derbise et al. (2007)
	φRSS1 – R. solanacearum MAFF 106603 and MAFF 106611	Enhanced virulence of bacterial host leading to an early onset of wilting and spread of infection in tomato Increase in extracellular polysaccharide (EPS) production, cell surface hydrophobicity, cell aggregation and density; pathogenicity traits (increase in twitching motility and pilin production; early expression of phcA global virulence regulator)	Addy, Askora, Kawasaki, Fujie, and Yamada (2012a)
	VPIφ – V. cholera strains (N16961 and 395)	Evolution of potentially pathogenic, nonepidemic strains (non‐O1 and non‐O139) Horizontal transfer of toxin‐coregulated pilus gene (tcpA) residing in vibrio pathogenicity island	Li, Kotetishvili, Chen, and Sozhamannan (2003)
	fs2 – V. cholera O1	Increase in virulence and reduction in colonizing ability; increase in in vivo production of cholera toxin (CT) and phage CTXf Lateral transfer of rstC gene in V. cholerae O1 and O139; reduction in type IV fimbrial production and hemagglutination activity; increase in in vivo detachment of cells	Nguyen et al. (2008)
	Cf1c – X. campestris pv. Citri	Evolution of virulent pathogenic variants	Kuo et al. (1991)
	Pf4 – P. aeruginosa PAO1	Increase in colonization potential to new surfaces Triggering of attachment and biofilm formation; development of small colony variants (SCVs)	Webb et al. (2004)
	f1, c2 – Enterobacteria sp.	Development of superinfective forms due to high frequency of mutations Development of small colony variant; loss of cell viability and reduction in rates of RNA and protein synthesis	Kuo, Yang, Chen, and Kuo (2000)
	Pf – P. aeruginosa	Increase in transmissibility, pathogenic persister phenotype Increased cellular viscosity, aggregation and adhesion; promotion of liquid crystalline organization of biofilm matrix	Secor et al. (2015)
	φRSS1, φRSM1 (Ff‐type) – R. solanacearum C319; Ps29	Enhanced virulence to cause early onset of wilting in tobacco plants	Yamada et al. (2007)
	Pf1 – Pseudomonas aeruginosa PAO1	Development of antimicrobial tolerant biofilms Transfer of genes within biofilms due to phage induction	Whiteley et al. (2001)
	PE226 – R. solanacearum SL341	Emergence of high virulence to infect wide host range (pepper, tomato and tobacco); Acquiring of zot‐like protein (putative bacterial virulence factor)	Murugaiyan et al. (2010)
	YpfΦ – Y. pestis biovar Orientalis (CO92), Antiqua (IP550‐HC1), Medievalis (IP1865‐12)	Emergence of highly virulent and pathogenic strain by transformation of Y. pseudotuberculosis after horizontal acquisition of filamentous phage YpfΦ over the last 20,000 years	Chouikha et al. (2010)
Enhance host cell aggregation for colonization but reduced virulence	XacF1 – Xanthomonas axonopodis pv. citri	Reduction in colonization ability, biofilm formation and virulence to cause citrus canker Reduction in swimming, swarming, and twitching motility; low levels of PilA type IV pili; reduction in cell adhesion due to EPS production; slow growth rate	Ahmad et al. (2014)
	φRSM1 and φRSM3 – R. solanacearumMAFF 106603 and MAFF 106611	Loss of virulence to show wilting symptoms in tomato Reduction of twitching motility, type IV pili, β‐1,4‐endoglucanase activity, EPS production; and expression of pathogenicity genes (egl, pehC, phcA, phcB, pilT, and hrpB)	Addy et al. (2012b)
	φRSM (φRSM3, φRSM4) – R. solanacearum (MAFF730139, MAFF106611 UW551 )	Extreme reduction in pathogenic potential to cause wilting in tomato Increase cell aggregation and colony size	Askora et al. (2009)
Phages in theory of community assembly and evolution: As an agent to influence evolutionary potential of bacterial inoculant and trigger microbial community development
Reduction in conjugative ability and plasmid transfer function	f1 – E. coli K38	• Number of defective F‐pili	Boeke et al. (1982)
	Ike – E. coli K12 RM98	• Alteration in cell membrane proteins	Iyer , Darby, and Holland, (1976)
Diversification in Isogenic population	M13 – E. coli	• Induction of high variability in individual viral production than other phenotypic traits in isogenic bacterial population	De Paepe, De Monte, Robert, Lindner, and Taddei et al. (2010)
Maintenance of conjugation rate and spread of antibiotic resistance within population	φM13 – E. coli W6	• Reduction in conjugation efficiency by ~10%	Wan and Goddard (2012)
	φM13‐km – E. coli TOP10F	• Reduction in average number of pili; decrease in conjugation rate with increase in pfu/ml	Lin et al. (2011)
Evolution and Development of superinfective forms and virulent pathogenic variants due to high frequency of mutations	Cf1c – X. campestris pv. Citri	• Variation in gene structure and sequence	Kuo et al. (1991)
	f1, c2 – Enterobacteria sp.	• Loss of cell viability and reduction in rates of RNA and protein synthesis	Kuo et al. (2000)