ArticlePublisher preview available

Aerobic degradation of dichlorinated dibenzo-p-dioxin and dichlorinated dibenzofuran by bacteria strains obtained from tropical contaminated soil

April 2020
Biodegradation 31(1-2)

April 2020
31(1-2)

DOI:10.1007/s10532-020-09898-8

Authors:

Salametu Saibu

Lagos State University

Sunday Adebusoye

University of Lagos

Ganiyu Oladunjoye Oyetibo

University of Lagos

Bacterial diversity and aerobic catabolic competence of dioxin-degrading bacterial strains isolated from a polluted soil in the tropics were explored. Isolation of bacteria occurred after 12 months of consecutive enrichment, with dioxin congeners serving as the only sources of carbon and energy. Seventeen strains that were isolated were subsequently screened for dioxin metabolic competence. Among these isolates, five had unique amplified ribosomal DNA restriction analysis (ARDRA) patterns out of which two exhibiting good metabolic competence were selected for further investigation. The two strains were identified as Bacillus sp. SS2 and Serratia sp. SSA1, based on their 16S rRNA gene sequences. Bacterial growth co-occurred with dioxin disappearance and near stoichiometric release of chloride for one ring of the chlorinated congeners. The overall percentage removal of dibenzofuran (DF) by strain SS2 was 93.87%; while corresponding values for 2,8-dichlorodibenzofuran (2,8-diCDF) and 2,7-dichlorodibenzo-p-dioxin (2,7-diCDD) were 86.22% and 82.30% respectively. In the case of strain SSA1, percentage removal for DF, 2,8-diCDF and 2,7-diCDD were respectively 98.9%, 80.97% and 70.80%. The presence of two dioxin dioxygenase catabolic genes (dxnA1 and dbfA1) was investigated. Only the dbfA1 gene could be amplified in SS2 strain. Results further revealed that strain SS2 presented higher expression levels for the alpha-subunit of DF dioxygenase (dbfA1) gene during growth with dioxins. The expression level for dbfA1 gene was higher when growing on DF than on the other chlorinated analogs. This study gives an insight into dioxin degradation, with the catabolic potential of strains SS2 and SSA1 (an enteric bacterium) within the sub-Sahara Africa. It further shows that dioxin catabolic potential might be more prevalent in different groups of microorganisms than previously believed. Few reports have demonstrated the degradation of chlorinated congeners of dioxins, particularly from sub-Saharan African contaminated systems.

Pathways for metabolism of dibenzofuran through angular and lateral dioxygenation by Janibacter terrae strain XJ-1 as proposed by Jin et al. (2006) with some modifications with respect to gene expression data and metabolites encountered in strain SS2 as presented in this study. Dibenzofuran-4,4a-dioxygenase (i), 4,4a-dihydroxy-4-hydro-dibenzofuran dehydrogenase (ii), 2,2′,3-trihydroxybiphenyl dioxygenase (iii), 2-hydroxy-6-oxo-6-(2′-hydroxyphenyl)-hexa-2,4-dienoic acid hydrolase (iv), dibenzofuran-1,2-dioxygenase (v), 1,2-dihydroxy-1,2-dihydrodibenzofuran dehydrogenase (vi), 1,2-dihydroxydibenzofuran dioxygenase (vii), 2-hydroxy-4-(3′oxo-3′H-benzofuran-2′yliden)but-2-enoic acid hydrolase (viii), salicylic acid-5-hydroxylase (ix), salicylic acid-1-hydroxylase (x) and, catechol-2,3-dioxygenase (xi). The dbfA1 gene for expression of protein mediating the production of compounds 1 and 2 was well expressed in strain SS2 while chlorinated metabolites 3 and 4 (2-chlorohydroxymuconic acid) were recovered in the culture fluids all indicating angular pathway in the organism

…

Dendrogram representing the genetic relationships among the bacterial isolates with different band patterns based on ARDRA fingerprints. The data were sorted by using the UPGMA clustering method in PyElph software

…

Phylogenetic tree based on the 16S rRNA gene sequences of dioxin-degrading bacterial isolates (with asterisks) obtained from an incinerator waste dump site and reference sequences from GenBank. The tree was created with Mega software version X using the neighbor-joining algorithm with 500 bootstrap replications; bootstrap values less than 50% are shown at the branch nodes; the scale bars represents 20% sequence divergence. The 16S rRNA gene sequence of Janibacter sp. strain XJ-1 was used as outgroup reference The GenBank accession number of all sequences used to build the tree is given in parentheses

…

Growth dynamics of the of five isolates (Bacillus sp. SS2, open circle; Serrattia sp. SSA1, open square; Klebsiella sp. SSA7, open triangle; Bordetella sp. SSA6, Inverted triangle; Provetella sp. SSA5, open diamond) on DF. The organisms were grown in MS medium supplemented with 100 mg l⁻¹ of the substrate and cultivated for 24 h. No growth was observed in non-inoculate or heat-inactivated control flasks

…

Growth of bacterial strains in MS Medium supplemented with 150 mg l⁻¹ of DF as a sole source of carbon and energy under aerobic batch conditions. Growth is shown as an increase in total viable counts (filled circle) and decrease in concentration of DF (filled square) monitored by GC–MS. In controls with heat-inactivated cells (open square), substrate was not utilized a minimal abiotic loss occurred. Data points represent means of at least two replicate determinations. In some cases, error bars were eliminated to improve clarity

…

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ORIGINAL PAPER

Aerobic degradation of dichlorinated dibenzo-p-dioxin

and dichlorinated dibenzofuran by bacteria strains obtained

from tropical contaminated soil

Salametu Saibu .Sunday A. Adebusoye .Ganiyu O. Oyetibo .Debora F. Rodrigues

Received: 30 September 2019 / Accepted: 7 April 2020 / Published online: 27 April 2020

ÓSpringer Nature B.V. 2020

Abstract Bacterial diversity and aerobic catabolic

competence of dioxin-degrading bacterial strains

isolated from a polluted soil in the tropics were

explored. Isolation of bacteria occurred after

12 months of consecutive enrichment, with dioxin

congeners serving as the only sources of carbon and

energy. Seventeen strains that were isolated were

subsequently screened for dioxin metabolic compe-

tence. Among these isolates, ﬁve had unique ampliﬁed

ribosomal DNA restriction analysis (ARDRA) pat-

terns out of which two exhibiting good metabolic

competence were selected for further investigation.

The two strains were identiﬁed as Bacillus sp. SS2 and

Serratia sp. SSA1, based on their 16S rRNA gene

sequences. Bacterial growth co-occurred with dioxin

disappearance and near stoichiometric release of

chloride for one ring of the chlorinated congeners.

The overall percentage removal of dibenzofuran (DF)

by strain SS2 was 93.87%; while corresponding values

for 2,8-dichlorodibenzofuran (2,8-diCDF) and 2,7-

dichlorodibenzo-p-dioxin (2,7-diCDD) were 86.22%

and 82.30% respectively. In the case of strain SSA1,

percentage removal for DF, 2,8-diCDF and 2,7-

diCDD were respectively 98.9%, 80.97% and

70.80%. The presence of two dioxin dioxygenase

catabolic genes (dxnA1 and dbfA1) was investigated.

Only the dbfA1 gene could be ampliﬁed in SS2 strain.

Results further revealed that strain SS2 presented

higher expression levels for the alpha-subunit of DF

dioxygenase (dbfA1) gene during growth with dioxins.

The expression level for dbfA1 gene was higher when

growing on DF than on the other chlorinated analogs.

This study gives an insight into dioxin degradation,

with the catabolic potential of strains SS2 and SSA1

(an enteric bacterium) within the sub-Sahara Africa. It

further shows that dioxin catabolic potential might be

more prevalent in different groups of microorganisms

than previously believed. Few reports have demon-

strated the degradation of chlorinated congeners of

dioxins, particularly from sub-Saharan African con-

taminated systems.

Keywords Biodegradation Dioxins Dioxygenase

gene Contaminated soil Serratia sp. Bacillus sp.

S. Saibu S. A. Adebusoye (&)G. O. Oyetibo

Department of Microbiology, Faculty of Science,

University of Lagos, Akoka, Yaba, Lagos, Nigeria

e-mail: sadebusoye@yahoo.com;

sadebusoye@unilag.edu.ng

S. Saibu

e-mail: salametu.saibu@students.unilag.edu.ng

G. O. Oyetibo

e-mail: goyetibo@unilag.edu.ng

S. Saibu D. F. Rodrigues

Department of Civil and Environmental Engineering,

University of Houston, Houston, TX 77204-4003, USA

e-mail: dfrigirodrigues@uh.edu

123

Biodegradation (2020) 31:123–137

https://doi.org/10.1007/s10532-020-09898-8(0123456789().,-volV)(0123456789().,-volV)

Content courtesy of Springer Nature, terms of use apply. Rights reserved.

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