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. 2020 Oct 30;10(11):320.
doi: 10.3390/membranes10110320.

Diversity of Acyl Homoserine Lactone Molecules in Anaerobic Membrane Bioreactors Treating Sewage at Psychrophilic Temperatures

Shamas Tabraiz  1 , Burhan Shamurad  1 , Evangelos Petropoulos  1 , Alex Charlton  2 , Obaidullah Mohiudin  1 , Mohammad Danish Khan  1 , Emeka Ekwenna  3 , Paul Sallis  1
Affiliations

Diversity of Acyl Homoserine Lactone Molecules in Anaerobic Membrane Bioreactors Treating Sewage at Psychrophilic Temperatures

Shamas Tabraiz et al. Membranes (Basel). .

Abstract

This study explores the types of acyl homoserine lactone (AHL) and their concentrations in different compartments of different conventional anaerobic bioreactors: (i) an upflow anaerobic membrane bioreactor (UAnMBR, biofilm/mixed liquor (sludge)); (ii) an anaerobic membrane bioreactor (AnMBR, biofilm/mixed liquor (sludge)); and (iii) an upflow sludge blanket (UASB, sludge only), all operating at 15 °C. Ten types of the AHL, namely C4-HSL, 3-oxo-C4-HSL, C6-HSL, 3-oxo-C6-HSL, C8-HSL, 3-oxo-C8-HSL, C10-HSL, 3-oxo-C10-HSL, C12-HSL, and 3-oxo-C12-HSL, which were investigated in this study, were found in UAnMBR and UASB, whilst only six of them (C4-HSL, 3-oxo-C4-HSL, C8-HSL, C10-HSL, 3-oxo-C10-HSL, and C12-HSL) were found in AnMBR. Concentrations of total AHL were generally higher in the biofilm than the sludge for both membrane bioreactors trialed. C10-HSL was the predominant AHL found in all reactors (biofilm and sludge) followed by C4-HSL and C8-HSL. Overall, the UAnMBR biofilm and sludge had 10-fold higher concentrations of AHL compared to the AnMBR. C10-HSL was only correlated with bacteria (p < 0.05), whilst other types of AHL were correlated with both bacteria and archaea. This study improves our understanding of AHL-mediated Quorum Sensing (QS) in the biofilms/sludge of UAnMBR and AnMBR, and provides new information that could contribute to the development of quorum quenching anti-fouling strategies in such systems.

Keywords: acyl homoserine lactone; anaerobic membrane bioreactor; quorum sensing.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Chemical oxygen demand (COD) percentage removal efficacies monitored in the last two months of operation to access the steady-state conditions of all the bioreactors. Sample were taken after every 5 days (n = 12). The error bar represents standard deviation.
Figure 2
Figure 2
Acyl homoserine lactone (AHL) concentrations in the biofilm (ng kg−1) and sludge (mg L−1) of (a) UAnMBR and UASB (sludge only), (b) AnMBR (error bars show standard deviation of replicates; n = 2); the y-axis is a log scale. AHL abbreviations are; C4: C4-HSL; C6: C6-HSL; C8: C8-HSL; C10: C10-HSL; C12: C12-HSL; OC4: 3-oxo-C4-HSL; OC6: 3-oxo-C6-HSL; OC8: 3-oxo-C8-HSL; OC10: 3-oxo-C10-HSL; OC12: 3-oxo-C12-HSL. The abbreviation of ND; not detected.
Figure 2
Figure 2
Acyl homoserine lactone (AHL) concentrations in the biofilm (ng kg−1) and sludge (mg L−1) of (a) UAnMBR and UASB (sludge only), (b) AnMBR (error bars show standard deviation of replicates; n = 2); the y-axis is a log scale. AHL abbreviations are; C4: C4-HSL; C6: C6-HSL; C8: C8-HSL; C10: C10-HSL; C12: C12-HSL; OC4: 3-oxo-C4-HSL; OC6: 3-oxo-C6-HSL; OC8: 3-oxo-C8-HSL; OC10: 3-oxo-C10-HSL; OC12: 3-oxo-C12-HSL. The abbreviation of ND; not detected.
Figure 3
Figure 3
(a) Polysaccharides in soluble extracellular polymeric substance (S_EPS), loosely bound extracellular polymeric substance (LB_EPS), and tightly bound extracellular polymeric substance (TB_EPS) in AnMBR_BF and UAnMBR_BF; (b) proteins in S_EPS, LB_EPS, and TB_EPS in AnMBR_BF and UAnMBR_BF; (c) polysaccharides in S-EPS, LB-EPS, and TB-EPS in AnMBR_S, UAnMBR_S, and UASB; (d) proteins in S_EPS, LB_EPS, and TB_EPS in AnMBR_S, UAnMBR_S, and UASB. The concentrations of the proteins and polysaccharides in the biofilms are reported in mg kg−1, while in the sludge, they are reported in mg L−1 (error bars represent standard deviation of replicates; n = 2). (e) Pearson correlation between proteins, polysaccharides, and AHL present in the biofilm and sludge of the AnMBR, UAnMBR, and UASB. S_EPS1: polysaccharides in soluble extracellular polymeric substances; LB.EPS1: polysaccharides in loosely bound extracellular polymeric substances; TB.EPS1: polysaccharides in tightly bound extracellular polymeric substances; S.EPS2: proteins in soluble extracellular polymeric substances; LB.EPS2: proteins in loosely bound extracellular polymeric substances; TB.EPS2: proteins in tightly bound extracellular polymeric substances. The asterisk (*) indicates p < 0.05. AHL abbreviations are; C4: C4-HSL; C6: C6-HSL; C8: C8-HSL; C10: C10-HSL; C12: C12-HSL; OC4: 3-oxo-C4-HSL; OC6: 3-oxo-C6-HSL; OC8: 3-oxo-C8-HSL; OC10: 3-oxo-C10-HSL; OC12: 3-oxo-C12-HSL.
Figure 3
Figure 3
(a) Polysaccharides in soluble extracellular polymeric substance (S_EPS), loosely bound extracellular polymeric substance (LB_EPS), and tightly bound extracellular polymeric substance (TB_EPS) in AnMBR_BF and UAnMBR_BF; (b) proteins in S_EPS, LB_EPS, and TB_EPS in AnMBR_BF and UAnMBR_BF; (c) polysaccharides in S-EPS, LB-EPS, and TB-EPS in AnMBR_S, UAnMBR_S, and UASB; (d) proteins in S_EPS, LB_EPS, and TB_EPS in AnMBR_S, UAnMBR_S, and UASB. The concentrations of the proteins and polysaccharides in the biofilms are reported in mg kg−1, while in the sludge, they are reported in mg L−1 (error bars represent standard deviation of replicates; n = 2). (e) Pearson correlation between proteins, polysaccharides, and AHL present in the biofilm and sludge of the AnMBR, UAnMBR, and UASB. S_EPS1: polysaccharides in soluble extracellular polymeric substances; LB.EPS1: polysaccharides in loosely bound extracellular polymeric substances; TB.EPS1: polysaccharides in tightly bound extracellular polymeric substances; S.EPS2: proteins in soluble extracellular polymeric substances; LB.EPS2: proteins in loosely bound extracellular polymeric substances; TB.EPS2: proteins in tightly bound extracellular polymeric substances. The asterisk (*) indicates p < 0.05. AHL abbreviations are; C4: C4-HSL; C6: C6-HSL; C8: C8-HSL; C10: C10-HSL; C12: C12-HSL; OC4: 3-oxo-C4-HSL; OC6: 3-oxo-C6-HSL; OC8: 3-oxo-C8-HSL; OC10: 3-oxo-C10-HSL; OC12: 3-oxo-C12-HSL.
Figure 4
Figure 4
(a) Non-metric multidimensional scaling (NMDS) plot of reactor communities, (b) relative abundance of the 30 most abundant bacteria; (c) relative abundance of the 20 most abundant archaea. AnMBR_BF is the biofilm from AnMBR, AnMBR_S is the sludge from AnMBR, UAnMBR_BF is the biofilm from UAnMBR, and UASB represents sludge from the UASB.
Figure 5
Figure 5
Canonical correspondence analysis (CCA) of acyl homoserine lactones (AHL) concentrations with (a) all archaea and (b) the 30 most abundant bacteria. AnMBR_BF is the biofilm from AnMBR, AnMBR_S is the sludge from AnMBR, UAnMBR_BF is the biofilm from UAnMBR, and UASB represents sludge from the UASB. AHL abbreviations are as follows; C4: C4-HSL; C6: C6-HSL; C8: C8-HSL; C10: C10-HSL; C12: C12-HSL; OC4: 3-oxo-C4-HSL; OC6: 3-oxo-C6-HSL; OC8: 3-oxo-C8-HSL; OC10: 3-oxo-C10-HSL; OC12: 3-oxo-C12-HSL.
Figure 6
Figure 6
Co-occurrence network of biofilm and sludge of all reactors at genus level and AHL concentrations. The modularity of the nodes is differentiated by colors at genus level and AHL concentration. Only strong (Pearson’s R > 0.8) and significant (p < 0.05) correlation connections were included, and nodes were labeled for genus (black) and AHL concentration (blue).
Figure 7
Figure 7
Percentage flux reduction in AnMBR and UAnMBR from the 100th (new membrane installed) to the 190th day.
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