<em>Mycobacterium avium</em> complex: Adherence as a way of life

Joseph O. Falkinham; Joseph O. Falkinham

doi:10.3934/microbiol.2018.3.428

AIMS Microbiology

2018, Volume 4, Issue 3: 428-438. doi: 10.3934/microbiol.2018.3.428

Previous Article Next Article

Review Special Issues

Mycobacterium avium complex: Adherence as a way of life

Joseph O. Falkinham ^,

Department of Biological Sciences, Virginia Tech, Blacksburg, Virginia 24061, USA

Received: 20 April 2018 Accepted: 08 June 2018 Published: 12 June 2018

Mycobacterium avium complex (MAC) organisms are waterborne, opportunistic pathogens whose source is natural waters and soils and proliferates and persists in premise plumbing, for example household and hospital plumbing. M. avium complex and other environmental mycobacteria grow slowly, not because their metabolism is slow, but because they synthesize long chain (C₆₀–C₈₀) fatty acids that make up its hydrophobic and impermeable outer membrane. There are costs and benefits to the presence of that lipid-rich outer membrane. One benefit is that cell-surface hydrophobicity drives M. avium complex cells to adhere to surfaces to reduce their interaction with charged ions in suspension; they are likely “biofilm pioneers”, adhering to a wide variety of surface materials. The result is that the slow-growing M. avium complex cells (1 gen/day at 37 °C) will not be washed out of any flowing system, whether a stream or plumbing in the built environment. Although the slow permeation of nutrients in M. avium complex organisms limits growth, they are also resistant to disinfectants, thus increasing their survival in water distribution systems, premise plumbing, and medical equipment. There are three components to the antimicrobial resistance of M. avium complex in biofilms: (1) innate resistance due to the hydrophobic, impermeable outer membrane, (2) residence in a matrix of extracellular polysaccharide, lipid, DNA, and protein that prevents access of antimicrobials to M. avium cells, and (3) an adaptive and transient increased resistance of biofilm-grown M. avium cells grown in biofilms. As expected M. avium in biofilms will display neutral, antagonistic, or beneficial interactions with other biofilm inhabitants. Methylobacterium spp., the common pink-pigmented, waterborne bacteria compete with M. avium for surface binding, suggested an approach to reducing M. avium biofilm formation and hence persistence in premise plumbing.
- mycobacteria,
- M. avium complex,
- MAC,
- adherence,
- hydrophobic,
- biofilm,
- disinfectant,
- antibiotic,
- methylobacteria
Citation: Joseph O. Falkinham. Mycobacterium avium complex: Adherence as a way of life[J]. AIMS Microbiology, 2018, 4(3): 428-438. doi: 10.3934/microbiol.2018.3.428

Related Papers:

Abstract

Mycobacterium avium complex (MAC) organisms are waterborne, opportunistic pathogens whose source is natural waters and soils and proliferates and persists in premise plumbing, for example household and hospital plumbing. M. avium complex and other environmental mycobacteria grow slowly, not because their metabolism is slow, but because they synthesize long chain (C₆₀–C₈₀) fatty acids that make up its hydrophobic and impermeable outer membrane. There are costs and benefits to the presence of that lipid-rich outer membrane. One benefit is that cell-surface hydrophobicity drives M. avium complex cells to adhere to surfaces to reduce their interaction with charged ions in suspension; they are likely “biofilm pioneers”, adhering to a wide variety of surface materials. The result is that the slow-growing M. avium complex cells (1 gen/day at 37 °C) will not be washed out of any flowing system, whether a stream or plumbing in the built environment. Although the slow permeation of nutrients in M. avium complex organisms limits growth, they are also resistant to disinfectants, thus increasing their survival in water distribution systems, premise plumbing, and medical equipment. There are three components to the antimicrobial resistance of M. avium complex in biofilms: (1) innate resistance due to the hydrophobic, impermeable outer membrane, (2) residence in a matrix of extracellular polysaccharide, lipid, DNA, and protein that prevents access of antimicrobials to M. avium cells, and (3) an adaptive and transient increased resistance of biofilm-grown M. avium cells grown in biofilms. As expected M. avium in biofilms will display neutral, antagonistic, or beneficial interactions with other biofilm inhabitants. Methylobacterium spp., the common pink-pigmented, waterborne bacteria compete with M. avium for surface binding, suggested an approach to reducing M. avium biofilm formation and hence persistence in premise plumbing.

References

[1]	Falkinham JO (2009) Surrounded by mycobacteria: nontuberculous mycobacteria in the human environment. J Appl Microbiol 107: 356–367. doi: 10.1111/j.1365-2672.2009.04161.x
[2]	Prevots DR, Marras TK (2015) Epidemiology of human pulmonary infection with nontuberculous mycobacteria: a review. Clin Chest Med 36: 13–34. doi: 10.1016/j.ccm.2014.10.002
[3]	Marras TK, Daley CL (2002) Epidemiology of human and pulmonary infection with nontuberculous mycobacteria. Clin Chest Med 23: 553–567. doi: 10.1016/S0272-5231(02)00019-9
[4]	Prince DS, Peterson DD, Steiner RM, et al. (1989) Infection with Mycobacterium avium complex in patients without predisposing conditions. N Engl J Med 321: 863–868. doi: 10.1056/NEJM198909283211304
[5]	Griffith DE, Aksamit T, Brown-Elliott BA, et al. (2007) An official ATS/IDSA statement: Diagnosis, treatment, and prevention of nontuberculous mycobacterial diseases. Am J Resp Crit Care 175: 367–416. doi: 10.1164/rccm.200604-571ST
[6]	Wallace RJ, Zhang Y, Brown-Elliott BA, et al. (2002) Repeat positive cultures in Mycobacterium intracellulare lung disease after macrolide therapy represent new infection in patients with nodular bronchiectasis. J Infect Dis 186: 266–173. doi: 10.1086/341207
[7]	Boyle DP, Zembower TR, Qi C (2016) Relapse versus reinfection of Mycobacterium avium complex pulmonary disease: patient characteristics and macrolide susceptibility. Ann Am Thorac Soc 13: 1956–1961. doi: 10.1513/AnnalsATS.201605-344BC
[8]	Wolinsky E (1995) Mycobacterial lymphadenitis in children: a prospective study of 105 nontuberculous cases with long-term follow up. Clin Infect Dis 20: 954–963. doi: 10.1093/clinids/20.4.954
[9]	Iivanainen E, Sallantaus T, Katila MJ, et al. (1999) Mycobacteria in runoff-waters from natural and drained peatlands. J Environ Qual 28: 1226–1234.
[10]	Falkinham JO, Parker BC, Gruft H (1980) Epidemiology of infection by nontuberculous mycobacteria. I. Geographic distribution in the eastern United States. Am Rev Respir Dis 121: 931–937.
[11]	Falkinham JO, Norton CD, LeChevallier MW (2001) Factors influencing numbers of Mycobacterium avium, Mycobacterium intracellulare, and other mycobacteria in drinking water distribution systems. Appl Environ Microbiol 67: 1225–1231. doi: 10.1128/AEM.67.3.1225-1231.2001
[12]	Falkinham JO (2011) Nontuberculous mycobacteria from household plumbing of patients with nontuberculous mycobacteria disease. Emerg Infect Dis 17: 419–424. doi: 10.3201/eid1703.101510
[13]	Falkinham JO, Iseman MD, de Haas P, et al. (2008) Mycobacterium avium in a shower linked to pulmonary disease. J Water Health 6: 209–213.
[14]	Feazel LM, Baumgartner LK, Peterson KL, et al. (2009) Opportunistic pathogens enriched in showerhead biofilms. P Natl Acad Sci USA 106: 16393–16399. doi: 10.1073/pnas.0908446106
[15]	Falkinham JO (2010) Hospital water filters as a source of Mycobacterium avium complex. J Med Microbiol 59: 1198–1202. doi: 10.1099/jmm.0.022376-0
[16]	Sax H, Bloemberg G, Hasse B, et al. (2015) Prolonged outbreak of Mycobacterium chimaera infection after open-chest heart surgery. Clin Infect Dis 61: 67–75. doi: 10.1093/cid/civ198
[17]	Mullis SN, Falkinham JO (2013) Adherence and biofilm formation of Mycobacterium avium, Mycobacterium intracellulare and Mycobacterium abscessus to household plumbing materials. J Appl Microbiol 115: 908–914. doi: 10.1111/jam.12272
[18]	George KL, Parker BC, Gruft H, et al. (1980) Epidemiology of infection by nontuberculous mycobacteria: II. Growth and survival in natural waters. Am Rev Respir Dis 122: 89–94.
[19]	Taylor RM, Norton CD, LeChevallier MW, et al. (2000) Susceptibility of Mycobacterium avium, Mycobacterium intracellulare, and Mycobacterium scrofulaceum to chlorine, chloramine, chlorine dioxide, and ozone. Appl Environ Microbiol 66: 1702–1705. doi: 10.1128/AEM.66.4.1702-1705.2000
[20]	Norton CD, LeChevallier MW, Falkinham JO (2004) Survival of Mycobacterium avium in a model distribution system. Water Res 38: 1457–1466. doi: 10.1016/j.watres.2003.07.008
[21]	Lewis AH, Falkinham JO (2015) Microaerobic growth and anaerobic survival of Mycobacterium avium, Mycobacterium intracellulare and Mycobacterium scrofulaceum. Int J Mycobacteriol 4: 25–30. doi: 10.1016/j.ijmyco.2014.11.066
[22]	Brennan PJ, Nikaido H (1995) The envelope of mycobacteria. Annu Rev Biochem 64: 29–63. doi: 10.1146/annurev.bi.64.070195.000333
[23]	Jarlier V, Nikaido H (1994) Mycobacterial cell wall: structure and role in natural resistance to antibiotics. FEMS Microbiol Lett 123: 11–18. doi: 10.1111/j.1574-6968.1994.tb07194.x
[24]	Falkinham JO, George KL, Parker BC, et al. (1984) In vitro susceptibility of human and environmental isolates of Mycobacterium avium, M. intracellulare, and M. scrofulaceum to heavy metal salts and oxyanions. Antimicrob Agents Ch 25: 137–139.
[25]	Chen CI, Griebe T, Srinivasan R, et al. (1993) Effects of various metal substrata on accumulation of Pseudomonas aeruginosa biofilms and the efficacy of monochloramine as a biocide. Biofouling 7: 241–251. doi: 10.1080/08927019309386256
[26]	Ojha A, Anand M, Bhatt A, et al. (2005) GroEL1: A dedicated chaperone involved in mycolic acid biosynthesis during biofilm formation in mycobacteria. Cell 123: 861–873. doi: 10.1016/j.cell.2005.09.012
[27]	Ojha AK, Baughn AD, Sambandan D, et al. (2008) Growth of Mycobacterium tuberculosis biofilms containing free mycolic acids and harbouring drug-tolerant bacteria. Mol Microbiol 69: 164–174. doi: 10.1111/j.1365-2958.2008.06274.x
[28]	De Beer D, Srinivasan R, Stewart PS (1994) Direct measurement of chlorine penetration into biofilms during disinfection. Appl Environ Microbiol 60: 4339–4344.
[29]	Birmes FS, Wolf T, Kohl TA, et al. (2017) Mycobacterium abscessus subsp. abscessus is capable of degrading Pseudomonas aeruginosa quinolone signals. Front Microbiol 8: 339.
[30]	Van Oss CJ, Gillman CF, Neumann AW (1975) Phagocytic engulfment and cell adhesiveness as cellular phenomena, New York: Marcel Dekker.
[31]	Lequette Y, Boels G, Clarisse M, et al. (2010) Using enzymes to remove biofilms of bacteria isolates sampled in the food-industry. Biofouling 26: 421–431. doi: 10.1080/08927011003699535
[32]	Muñoz-Egea MC, García-Pedrazuela M, Mahillo-Fernandez I, et al. (2016) Effect of antibiotics and antibiofilm agents in the ultrastructure and development of biofilms developed by nonpigmented rapidly growing mycobacteria. Microb Drug Resist 22: 1–6. doi: 10.1089/mdr.2015.0124
[33]	Steed KA, Falkinham JO (2006) Effect of growth in biofilms on chlorine susceptibility of Mycobacterium avium and Mycobacterium intracellulare. Appl Environ Microbiol 72: 4007–4100. doi: 10.1128/AEM.02573-05
[34]	Falkinham JO (2007) Growth in catheter biofilms and antibiotic resistance of Mycobacterium avium. J Med Microbiol 56: 250–254. doi: 10.1099/jmm.0.46935-0
[35]	Tortoli E, Rindi L, Garcia MJ, et al. (2004) Proposal to elevate the genetic variant MAC-A, included in the Mycobacterium avium complex, to species rank as Mycobacterium chimaera sp. nov. Int J Syst Evol Micr 54: 1277–1285. doi: 10.1099/ijs.0.02777-0
[36]	Wallace RJ, Iakhiaeva E, Williams MD, et al. (2013) Absence of Mycobacterium intracellulare and presence of Mycobacterium chimaera in household water and biofilms samples in the United States with Mycobacterium avium complex respiratory disease. J Clin Microbiol 51: 1747–1752. doi: 10.1128/JCM.00186-13
[37]	Kim E, Kinney WH, Ovrutsky AR, et al. (2014) A surface with a biomimetic micropattern reduces colonization of Mycobacterium abscessus. FEMS Microbiol Lett 359: 1–6. doi: 10.1111/1574-6968.12576
[38]	Kirschner RA, Parker BC, Falkinham JO (1992) Epidemiology of infection by nontuberculous mycobacteria. X. Mycobacterium avium, M. intracellulare, and M. scrofulaceum in acid, brown-water swamps of the southeastern United States and their association with environmental variables. Am Rev Respir Dis 145: 271–275.
[39]	Carter G, Wu M, Drummond DC, et al. (2003) Characterization of biofilm formation by clinical isolates of Mycobacterium avium. J Med Microbiol 52: 747–752. doi: 10.1099/jmm.0.05224-0
[40]	Freeman R, Geier H, Weigel KM, et al. (2006) Roles for cell wall glycopeptidolipid in surface adherence and planktonic dispersal of Mycobacterium avium. Appl Environ Microbiol 72: 7554–7558. doi: 10.1128/AEM.01633-06
[41]	Martínez A, Torello S, Kolter R (1999) Sliding motility in mycobacteria. J Bacteriol 181: 7331–7338.
[42]	Kelley ST, Theisen U, Angenent LT, et al. (2004) Molecular analysis of shower curtain biofilm microbes. Appl Environ Microbiol 70: 4187–4192. doi: 10.1128/AEM.70.7.4187-4192.2004
[43]	Falkinham JO, Williams MD, Kwait R, et al. (2016) Methylobacterium spp. as an indicator for the presence or absence of Mycobacterium spp. Int J Mycobacteriol 5: 240–243.
[44]	Muńoz-Egea MC, Ji P, Pruden A, et al. (2017) Inhibition of adherence of Mycobacterium avium to plumbing surface biofilms of Methylobacterium spp. Pathogens 6: 42. doi: 10.3390/pathogens6030042
[45]	Elbein AD, Pan YT, Pastuszak I, et al. (2003) New insights on trehalose: a multifunctional molecule. Glycobiology 13: 17R–27R. doi: 10.1093/glycob/cwg047

Reader Comments

your name:*

Email:*
© 2018 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)