Possible role of reactive chlorine in microbial antagonism and organic matter chlorination in terrestrial environments

Abstract

SummarySeveral studies have demonstrated that extensive formation of organically bound chlorine occurs both in soil and in decaying plant material. Previous studies suggest that enzymatic formation of reactive chlorine outside cells is a major source. However, the ecological role of microbial-induced extracellular chlorination processes remains unclear. In the present paper, we assess whether or not the literature supports the hypothesis that extracellular chlorination is involved in direct antagonism against competitors for the same resources. Our review shows that it is by no means rare that biotic processes create conditions that render biocidal concentrations of reactive chlorine compounds, which suggest that extracellular production of reactive chlorine may have an important role in antagonistic microbial interactions. To test the validity, we searched the UniprotPK database for microorganisms that are known to produce haloperoxidases. It appeared that many of the identified haloperoxidases from terrestrial environments are originating from organisms that are associated with living plants or decomposing plant material. The results of the in silico screening were supported by various field and laboratory studies on natural chlorination. Hence, the ability to produce reactive chlorine seems to be especially common in environments that are known for antibiotic-mediated competition for resources (interference competition). Yet, the ability to produce haloperoxidases is also recorded, for example, for plant endosymbionts and parasites, and there is little or no empirical evidence that suggests that these organisms are antagonistic.

The RclR Protein Is a Reactive Chlorine-specific Transcription Factor in Escherichia coli

“…The QuikChange site-directed mutagenesis kit (Stratagene), modified to use only a single primer and 35 cycles of amplification, was used to mutate pRCLR1 with primers [11], [12], [13], or [14] to yield plasmids pRCLR8, pRCLR9, pRCLR14, and pRCLR15, containing rclR alleles encoding RclR C21A , RclR C89A , RclR H42A , and RclR H75A , respectively. The same method was used to mutate pRCLR8 with primer [12], yielding plasmid pRCLR12, containing an rclR allele encoding RclR C21A,C89A .…”

“…HOCl Survival Assays-HOCl survival assays were performed as described previously (20). -TAC TAA GAT TGT TGG TGT TTG TAA TCA AAA ACC ACT CAG GAG TCT GAT ATG GTG TAG GCT GGA GCT GCT TC-3Ј [2] 5Ј-AAC TCC CGG AAT GCG GAT TAT CTT TGC CCT GAT TTC TGG CGG TTT TAT TCA CAT ATG AAT ATC CTC CTT AG-3Ј [3] 5Ј-CGT CTA TAG TCA TGA TGT CAA ATG AAC GCG TTT CGA CAG GAA ATC ATC ATG GTG TAG GCT GGA GCT GCT TC-3Ј [4] 5Ј-CTT TTC TCT GAG ACG CCA GAA TAT TTG TTC TGG CGT CTG ATT TTG AGT TTA CAT ATG AAT ATC CTC CTT AG-3Ј [5] 5Ј-TCT CTG TTA CTC TAT AAC TTC TTA ATC ACT TCA TTG ATG GTA TTT TAT ATG GTG TAG GCT GGA GCT GCT TC-3Ј [6] 5Ј-TAT CTC CCC GAC TTA ACA GGT GCA GGT ATT TTT CCA TTG TGA ACA TCC TTA CAT ATG AAT ATC CTC CTT AG-3Ј [7] 5Ј-TAA TAA TTC AAC CGC AAC AGC AGT ATT GTA TAA ATA AGG ATG TTC ACA ATG GTG TAG GCT GGA GCT GCT TC-3Ј [8] 5Ј-AGG GGG CCT GAC GCC TGA AAA AGT GAA CAA CAG ACA GTG TTC GGA TTA TCA CAT ATG AAT ATC CTC CTT AG-3Ј [9] 5Ј-TTC GAA TTC AGG AGT CTG ATA TGG ATG CCC-3Ј [10] 5Ј-CTT AAG CTT TCA GGG TGC AAG CTG TCT GA-3Ј [11] 5Ј-GAA CGA TCG ATA AGA ATG CGG TGT TAG GAA GTG ACT GG-3Ј [12] 5Ј-CGA CCT GTA TTG TCG CGG GCA CTC TTC GGT TG-3Ј [13] 5Ј-GAA TTA TCG GTT ATT CGT TGG GCG GCG TTA ACG CAA GGA GCG GC-3Ј [14] 5Ј-CCA CAA AAT TCA GCT GCG CGC CTG AGT CAT GTC G-3Ј [15] 5Ј-CAC GAT TGA TAA AAA CGC GGT CCT GGG TTC TGA CTG-3Ј [16] 5Ј-GAA TCC ACC TGC ATT GTT GCG GGT ACG CTG CGT CTG CAA C-3Ј [17] 5Ј-ACT GAG CGT TAT TCG TTG GGC GGC ACT GAC CCA GGG TGC A-3Ј [18] 5Ј-AGA ATA GTG CGG CGC GCC TGT CCC ACG TGG ATA A-3Ј [19] 5Ј-AAG AAC TTA CCT GGT CTT GAC ATC-3Ј [20] 5Ј-CAG TTT ATC ACT GGC AGT CTC CTT-3Ј [21] 5Ј-AAA AAC ATT CTC AGT TTG CTT CTG C-3Ј [22] 5Ј-CGC TAT TTG TAG ACG CAA CTT TGT T-3Ј [23] 5Ј-AGG GTT GGT ATG ACA GAA GAA CAA G-3Ј [24] 5Ј-TAT ATT GAT CAT CTC GTG GGA GTC A-3Ј [25] 5Ј-CAC TAT TAT CTG GCG TTA TGG CAT T-3Ј [26] 5Ј-TAT ACA ATA CTG CTG TTG CGG TTG-3Ј [27] 5Ј-TCT TTT ATG AAC ACC CGG AAG ACT A-3Ј [28] 5Ј-ATC AGT CCT CCC AAT AAA CCT AAC C-3Ј [29] 5Ј-GGT CCT TCT ATC ACT ACT TTC GCT CT-3Ј …”

“…Moreover, they are major bactericidal components of the oxidative burst of neutrophils (3,6,7) and are implicated in controlling bacterial colonization of epithelial surfaces (8 -10). There is now also increasing evidence that production of RCS is a common strategy among diverse eukaryotes for controlling bacterial populations (11,12). Understanding how bacteria sense and respond to RCS is therefore important for understanding the interactions between bacteria and their eukaryotic hosts, with obvious implications for the study of human health and disease.…”

Experimental Evidence of Large Changes in Terrestrial Chlorine Cycling Following Altered Tree Species Composition

“…The high chlorination rates and the large amounts of Cl org found, 13 and a large number of organisms being able to mediate chlorination (e.g., refs 14−16), indicates that the chlorine cycling is ubiquitous and may also have fundamental but yet unknown ecological implications. 17,18 In addition, the radioisotope 36 Cl has recently caused concerns due to its presence in radioactive waste and its long half-life (301 000 years). The fact that Cl are physiologically important for humans and other organisms, for example, in cellular ion balances, 19 and the potentially rapid uptake of 36 Cl by plants and in the end humans, makes it desirable to account for in 36 Cl radioactive risk assessment models.…”

Chlorine Cycling in Terrestrial Environments

“…hypochlorous acid, HOCl), which causes the unspecific chlorination of various organic compounds (Hoekstra, 1999;van Pée & Unversucht, 2003). It has been speculated that this unspecific extracellular function may play a role in microbial antagonism (Bengtson et al, 2009) or represent a way to handle oxygen stress (Bengtson et al, 2013).…”