The overproduction of 2,4-DTBP accompanying to the lack of available form of phosphorus during the biodegradative utilization of aminophosphonates by Aspergillus terreus

Lenartowicz, Paweł; Kafarski, Paweł; Lipok, Jacek

doi:10.1007/s10532-014-9716-z

Original Paper
Published: 12 November 2014

The overproduction of 2,4-DTBP accompanying to the lack of available form of phosphorus during the biodegradative utilization of aminophosphonates by Aspergillus terreus

Paweł Lenartowicz¹,
Paweł Kafarski¹ &
Jacek Lipok¹

Biodegradation volume 26, pages 65–76 (2015)Cite this article

411 Accesses
4 Citations
Metrics details

Abstract

Although information about the ability of some filamentous fungi to biodegrade organophosphonates is available, the knowledge about accompanying changes in fungal metabolism is very limited. The aim of our study was to determine the utilization of the chosen, structurally diverse aminophosphonates by Aspergillus terreus (Thom), in the context of the behaviour of this fungus while growing in unfavourable conditions, namely the lack of easily available phosphates. We found that all the studied compounds were utilized by fungus as nutritive sources of phosphorus, however, their effect on the production of fungal biomass depended on their structure. We also observed an interesting change in the metabolism of A. terreus; namely the overproduction of 2,4-di-tert-butylphenol (2,4-DTBP), which is known to possess fungistatic activity. In the case of our study, the biosynthesis of this compound was induced by phosphorus starvation, caused either by the lack of that element in the medium, or the poor degradation of phosphonate.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

Adams MM, Gomez-Garcia MR, Grossman AR, Bhaya D (2008) Phosphorus deprivation responses and phosphonate utilization in a thermophilic Synechococcu sp. from microbial mats. J Bacteriol 190:8171–8184. doi:10.1128/JB.01011-08
CAS PubMed Central PubMed Article Google Scholar
Brauer MJ, Yuan J, Bennett BD, Lu W, Kimball E, Botstein D, Rabinowitz JD (2006) Conservation of the metabolomic response to starvation across two divergent microbes. PNAS 103:19302–19307. doi:10.1073/pnas.0609508103
CAS PubMed Central PubMed Article Google Scholar
Bujacz B, Wieczorek P, Krzyśko-Łupicka T, Gołąb Z, Lejczak B, Kafarski P (1995) Organophosphonate utilization by the wild-type strain of Penicillium notatum. Appl Environ Microbiol 61:2905–2910
CAS PubMed Central PubMed Google Scholar
Caccavo F, Ramsing NB, Costerton JW (1996) Morphological and metabolic responses to starvation by the dissimilatory metal-reducing bacterium Shewanella alga BrY. Appl Environ Microbiol 62:4678–4682
CAS PubMed Central PubMed Google Scholar
Carvalho MB, Martins I, Leitao MC, Garcia H, Rodrigues C, Romao VS, McLellan I, Hursthouse A, Pereira CS (2009) Screening pentachlorophenol degradation ability by environmental fungal strains belonging to the phyla Ascomycota and Zygomycota. J Ind Microbiol Biotechnol 36:1249–1256. doi:10.1007/s10295-009-0603-2
CAS PubMed Article Google Scholar
Castro JV, Peralba MCR, Ayub MAZ (2007) Biodegradation of the herbicide glyphosate by filamentous fungi in platform shaker and batch bioreactor. J Environ Sci Health B 42:883–886. doi:10.1080/03601230701623290
CAS PubMed Article Google Scholar
Dhami S, Sanchita, Maurya A, Samad A, Srivastava SK, Sharma A, Patra DD (2014) Purification, characterization, and in vitro activity of 2,4-di-tert-butylphenol from Pseudomonas monteilii PsF84: conformational and molecular docking studies. J Agric Food Chem 62:6138–6146. doi:10.1021/jf5001138
Article Google Scholar
Forlani G, Prearo V, Wieczorek D, Kafarski P, Lipok J (2011) Phosphonate degradation by Spirulina strains: cyanobacterial biofilters for the removal of anticorrosive polyphosphonates from wastewater. Enzym Microb Technol 48:299–305. doi:10.1016/j.enzmictec.2010.12.005
CAS Article Google Scholar
Fuqua C, Greenberg EP (1998) Self perception in bacteria: quorum sensing with acylated homoserine lactones. Curr Opin Microbiol 1:183–189
CAS PubMed Article Google Scholar
Han TL, Cannon RD, Villas-Boas SG (2011) The metabolic basis of Candida albicans morphogenesis and quorum sensing. Fungal Genet Biol 48:747–763. doi:10.1016/j.fgb.2011.04.002
CAS PubMed Article Google Scholar
Hogan DA (2006) Talking to themselves: autoregulation and quorum sensing in fungi. Eukaryot Cell 5:613–619. doi:10.1128/EC.5.4.613-619.2006
CAS PubMed Central PubMed Article Google Scholar
http://www.zschimmer-schwarz.com/Phosphonates/1-158.Amino-tris.html Accessed 04 Nov 2014
http://www.zschimmer-schwarz.com/Phosphonates/1-162.Hexamethylenediamine-tetra.html Accessed 04 Nov 2014
Jung J, Noh J, Park W (2011) Physiological and metabolic responses for hexadecane degradation in Acinetobacter oleivorans DR1. J Microbiol 49:208–215. doi:10.1007/s12275-011-0395-8
CAS PubMed Article Google Scholar
Klement T, Buchs J (2013) Itaconic acid—a biotechnological process in change. Bioresour Technol 135:422–431. doi:10.1016/j.biortech.2012.11.141
CAS PubMed Article Google Scholar
Klimek-Ochab M, Lejczak B, Forlani G (2003) A metal-independent hydrolase from a Penicillium oxalicum strain able to use phosphonoacetic acid as the only phosphorus source. FEMS Microbiol Lett 222:205–209. doi:10.1016/S0378-1097(03)00301-X
CAS PubMed Article Google Scholar
Klimek-Ochab M, Obojska A, Picco AM, Lejczak B (2007) Isolation and characterization of two new microbial strains capable of degradation of the naturally occurring organophosphonate—ciliatine. Biodegradation 18:223–231. doi:10.1007/s10532-006-9057-7
CAS PubMed Article Google Scholar
Klimek-Ochab M, Much A, Żymańczyk-Duda E (2014) 2-Aminoethylphosphonate utilization by the cold-adapted Geomyces pannorum P11 strain. Curr Microbiol 68:330–335. doi:10.1007/s00284-013-0485-4
CAS PubMed Central PubMed Article Google Scholar
Knepper TP (2003) Synthetic chelating agents and compounds exhibiting complexing properties in the aquatic environment. Trends Anal Chem 22:708–724. doi:10.1016/S0165-9936(03)01008-2
CAS Article Google Scholar
Krzyśko-Łupicka T, Orlik A (1997) The use of glyphosate as the sole source of phosphorus or carbon for the selection of soil-borne fungal strains capable to degrade this herbicide. Chemosphere 34:2601–2605
Article Google Scholar
Krzyśko-Łupicka T, Strof W, Kubś K, Skorupa M, Wieczorek P, Lejczak B, Kafarski P (1997) The ability of soil-borne fungi to degrade organophosphonate carbon-to-phosphorus bonds. Appl Microbiol Biotechnol 48:549–552
PubMed Article Google Scholar
Li Z, Nair SK (2012) Quorum sensing: how bacteria can coordinate activity and synchronize their response to external signals? Protein Sci 21:1403–1417. doi:10.1002/pro.2132
CAS PubMed Central PubMed Article Google Scholar
Lipok J, Cierpicki T, Kafarski P (2002) Degradation of amino-(3-methoxyphenyl)- methanephosphonic acid by Alternaria sp. Phosphorus Sulphur Silicon 177:1657–1660. doi:10.1080/10426500212319
CAS Article Google Scholar
Lipok J, Wieczorek D, Jewginski M, Kafarski P (2009) Prospects of in vivo P-31 NMR method in glyphosate degradation studies in whole cell system. Enzym Microb Technol 44:11–16. doi:10.1016/j.enzmictec.2008.09.011
CAS Article Google Scholar
Loh KC, Cao B (2008) Paradigm in biodegradation using Pseudomonas putida–a review of proteomics studies. Enzym Microb Technol 43:1–12. doi:10.1016/j.enzmictec.2008.03.004
CAS Article Google Scholar
Lopez JLC, Sanchez Perez JA, Fernandez Sevilla JM, Rodriguez Porcel EM, Chisti Y (2005) Pellet morphology, culture rheology and lovastatin production in cultures of Aspergillus terreus. J Biotechnol 116:61–77
Article Google Scholar
Madhusudhan KT, McLaughlin R, Komori N, Matsumoto H (2003) Identification of a major protein upon phosphate starvation of Pseudomonas aeruginosa PAO1. J Basic Microbiol 43:36–46. doi:10.1002/jobm.200390002
CAS PubMed Article Google Scholar
Nitsche BM, Jorgensen TR, Akeroyd M, Meyer V, Ram AFJ (2012) The carbon starvation response of Aspergillus niger during submerged cultivation: insights from the transcriptome and secretome. BMC Genomics 13:380. doi:10.1186/1471-2164-13-380
CAS PubMed Central PubMed Article Google Scholar
Pollack JK, Li ZJ, Marten MR (2008) Fungal mycelia show lag time before re-growth on endogenous carbon. Biotechnol Bioeng 100:458–465. doi:10.1002/bit.21779
CAS PubMed Article Google Scholar
Quinn JP, Kulakova AN, Cooley NA, McGrath JW (2007) New ways to break an old bond: the bacterial carbon–phosphorus hydrolases and their role in biogeochemical phosphorus cycling. Environ Microbiol 9:2392–2400. doi:10.1111/j.1462-2920.2007.01397.x
CAS PubMed Article Google Scholar
Raina S, Odell M, Keshavarz T (2010) Quorum sensing as a method for improving sclerotiorin production in Penicillium sclerotiorum. J Biotechnol 148:91–98. doi:10.1016/j.jbiotec.2010.04.009
CAS PubMed Article Google Scholar
Raina S, De Vizio D, Palonen EK, Odell M, Brandt AM, Soini JT, Keshavarz T (2012) Is quorum sensing involved in lovastatin production in the filamentous fungus Aspergillus terreus? Process Biochem 47:843–852. doi:10.1016/j.procbio.2012.02.021
CAS Article Google Scholar
Sang MK, Kim KD (2012) The volatile-producing Flavobacterium johnsoniae strain GSE09 shows biocontrol activity against Phytophthora capsici in pepper. J Appl Microbiol 113:383–398. doi:10.1111/j.1365-2672.2012.05330.x
CAS PubMed Article Google Scholar
Sang MK, Do Kim J, Kim BS, Kim KD (2011) Root treatment with rhizobacteria antagonistic to Phytophthora blight affects anthracnose occurrence, ripening, and yield of pepper fruit in the plastic house and field. Phytopathology 101:666–678. doi:10.1094/PHYTO-08-10-0224
CAS PubMed Article Google Scholar
Schwarz R, Forchhammer K (2005) Acclimation of unicellular cyanobacteria to macronutrient deficiency: emergence of a complex network of cellular responses. Microbiology 151:2503–2514. doi:10.1099/mic.0.27883-0
CAS PubMed Article Google Scholar
Sobera M, Wieczorek P, Lejczak B, Kafarski P (1997) Organophosphonate utilization by the wild-type strain of Cladosporium resinae. Toxicol Environ Chem 61:229–235. doi:10.1080/02772249709358488
CAS Article Google Scholar
Staszczak M (2008) The role of the ubiquitin-proteasome system in the response of the ligninolytic fungus Trametes versicolor to nitrogen deprivation. FGB 45:328–337. doi:10.1016/j.fgb.2007.10.017
CAS Article Google Scholar
Studnik H, Liebsch S, Forlani G, Wieczorek D, Kafarski P, Lipok J (2015) Amino polyphosphonates—chemical features and practical uses, environmental durability and biodegradation. New Biotechnol 32:1–6. doi:10.1016/j.nbt.2014.06.007
CAS Article Google Scholar
Tayung K, Barik BP, Jha DK (2010) Antifungal activity and biocontrol potential of metabolite produced by an endophytic Fusarium (MTCC-9622) against some postharvest pathogens. J Agric Technol 6:409–419
Google Scholar
Ternan NG, McGrath JW, McMullan G, Quinn JP (1998) Organophosphonates: occurrence, synthesis and biodegradation by microorganisms. World J Microbiol Biotechnol 14:635–647
CAS Article Google Scholar
Tseng CH, Tang SL (2014) Marine microbial metagenomics: from individual to the environment. Int J Mol Sci 15:8878–8892. doi:10.3390/ijms15058878
PubMed Central PubMed Article Google Scholar
Wariishi H (2000) Fungal metabolism of environmentally persistent compounds: substrate recognition and metabolic response. Biotechnol Bioprocess Eng 5:422–430
CAS Article Google Scholar
Xie X, Wilkinson HH, Correa A, Lewis ZA, Bell-Pedersen D, Ebbole DJ (2004) Transcriptional response to glucose starvation and functional analysis of a glucose transporter of Neurospora crassa. FGB 41:1104–1119. doi:10.1016/j.fgb.2004.08.009
CAS Article Google Scholar
Zboińska E, Maliszewska I, Lejczak B, Kafarski P (1992) Degradation of organophosphonates by Penicillium citrinum. Lett Appl Microbiol 15:269–272
Article Google Scholar
Zeinali M, Vossoughi M, Ardestani SK, Babanezhad E, Masoumian M (2007) Hydrocarbon degradation by thermophilic Nocardia otitidiscaviarum strain TSH1: physiological aspects. J Basic Microbiol 47:534–539. doi:10.1002/jobm.200700283
CAS PubMed Article Google Scholar

Download references

Acknowledgments

This work was supported by Polish Ministry of Science and Higher Education in the frame of the National Science Centre Grant No. UMO-2011/01/B/NZ9/04722. Pawel Lenartowicz is a recipient of a Ph.D. scholarship under a project funded by the European Social Fund.

Author information

Affiliations

Faculty of Chemistry, Opole University, Oleska 48, 45-052, Opole, Poland
Paweł Lenartowicz, Paweł Kafarski & Jacek Lipok

Authors

Paweł Lenartowicz
View author publications
You can also search for this author in PubMed Google Scholar
Paweł Kafarski
View author publications
You can also search for this author in PubMed Google Scholar
Jacek Lipok
View author publications
You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jacek Lipok.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Lenartowicz, P., Kafarski, P. & Lipok, J. The overproduction of 2,4-DTBP accompanying to the lack of available form of phosphorus during the biodegradative utilization of aminophosphonates by Aspergillus terreus . Biodegradation 26, 65–76 (2015). https://doi.org/10.1007/s10532-014-9716-z

Download citation

Received: 30 July 2014
Accepted: 06 November 2014
Published: 12 November 2014
Issue Date: February 2015
DOI: https://doi.org/10.1007/s10532-014-9716-z

Keywords

Filamentous fungi
Aspergillus terreus
Phosphonate utilization
2,4-di-tert-butylphenol