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Minireview the Behavior and Significance of Degradative Microbes Environ. Vol. 25, No. 4, 253–265, 2010 http://wwwsoc.nii.ac.jp/jsme2/ doi:10.1264/jsme2.ME10155 Minireview The Behavior and Significance of Degradative Plasmids Belonging to Inc Groups in Pseudomonas within Natural Environments and Microcosms MASAKI SHINTANI1,2, YURIKA TAKAHASHI2, HISAKAZU YAMANE2, and HIDEAKI NOJIRI2* 1Bioresource Center, Japan Collection of Microorganisms (BRC-JCM), Riken, 2–1 Hirosawa, Wako, Saitama 351–0198, Japan; and 2Biotechnology Research Center, University of Tokyo, 1–1–1 Yayoi, Bunkyo-ku, Tokyo 113–8657, Japan (Received August 3, 2010—Accepted September 30, 2010—Published online October 21, 2010) Over the past few decades, degradative plasmids have been isolated from bacteria capable of degrading a variety of both natural and man-made compounds. Degradative plasmids belonging to three incompatibility (Inc) groups in Pseudomonas (IncP-1, P-7, and P-9) have been well studied in terms of their replication, maintenance, and capacity for conjugative transfer. The host ranges of these plasmids are determined by replication or conjugative transfer systems. The host range of IncP-1 is broad, that of IncP-9 is intermediate, and that of IncP-7 is narrow. To understand the behavior of these plasmids and their hosts in various environments, the survivability of inocula, stability or trans- ferability, and efficiency of biodegradation in environments and microcosms have been monitored. The biodegradation and plasmid transfer in various environments have been observed for all three groups, although the kinds of trans- conjugants differed with the Inc groups. In some cases, the deletion and amplification of catabolic genes acted to reduce the production of toxic catabolic intermediates, or to increase the activity on a particular catabolic pathway. The combination of degradative genes, the plasmid backbone of each Inc group, and the host of the plasmids is key to the degraders adapting to various hosts or to heterogeneous environments. Key words: degradative plasmid, IncP plasmid, conjugative transfer, bioaugmentation Introduction microorganisms may become attenuated (relative to the ini- tial inoculum) during growth at contaminated sites, which is Plasmids are bacterial mobile genetic elements that facili- particularly true in soil. Adequate dispersion of biodegrada- tate rapid evolution and adaptation by conjugative transfer tive microorganisms over contaminated areas is also prob- between bacterial cells in the natural environment. To date lematic. To overcome these problems, ‘gene bioaugmenta- (the end of Sept. 2010), the nucleotide sequences of 2178 plas- tion’ or ‘plasmid-mediated bioaugmentation’ (4, 7, 23, 82), mids have been determined and deposited in the NCBI data- the introduction of appropriate degradative plasmids con- base (http://www.ncbi.nlm.nih.gov/genomes/genlist.cgi?taxid tained within a microbial host, has been attempted. The =2&type=2&name=BacteriaPlasmids). Some plasmids con- rationale for this approach is that the degradative genes fer antibiotic resistance or virulence on the host bacterium, survive through incorporation into indigenous bacteria by while others—known as degradative plasmids—enhance the horizontal transfer. Additionally, plasmid transfer may result ability of the host cell to catabolize xenobiotic compounds in spatial movement of the catabolic genes through the soil, (33, 97). Here we use the term ‘xenobiotic compounds’ resulting in dissemination of the desired catabolic activity in a broad sense, to include “all compounds that are released into deeper layers. The artificial spread of specific genes in into the environment by human actions and whose concentra- the natural environment, however, may not be desirable. tions are higher than natural” (54). Over the past decade, Therefore, understanding the behavior of degradative plas- xenobiotic-degradative plasmids have been found in various mids and their hosts in natural microcosms is necessary biodegradative microorganisms isolated from geographically not only for elucidating bacterial evolution and adaptation diverse locations (25, 74, 75, 78, 113, 126). The genomes of systems, but also for evaluating the benefits and risks of some of these have been sequenced, and the capacity for bioaugmentation itself. replication, partition, and conjugative transfer were assessed Plasmids are classified into incompatibility (Inc) groups (35, 50, 52, 109). based on their replication and partition systems: two plas- Bioaugmentation is a method of removing xenobiotic mids belonging to the same Inc group are unable to coexist in compounds from contaminated sites via the introduction of one bacterial cell (i.e., they are incompatible). Members of biodegradative microorganisms. However, this method does the same group have a common plasmid backbone yielding not always successfully remove the contaminating sub- their basic features. There are at least 14 Inc groups in stances. Furthermore, the relationships among inoculum Pseudomonas, which are completely different from those of size, survival and fate of the inocula, and efficacy of con- E. coli, although some groups in each classification form a tamination removal remain unclear (32, 110). Biodegradative single Inc group; e.g., IncP-1 in the Pseudomonas plasmid classification corresponds to IncP in the Escherichia coli * Corresponding author. E-mail: [email protected]; plasmid classification (108). In this review, we use ‘Inc Tel: +81–3–5841–3064; Fax: +81–3–5841–8030. groups in Pseudomonas’ to indicate the groups IncP-1, P-2, 254 SHINTANI et al. P-3, and so on, although these plasmids do not necessarily replication in host Pseudomonas but is not functional in exist in Pseudomonas bacteria. Among the degradative E. coli or in other subdivisions of Proteobacteria (92, 129). plasmids, IncP-1, P-2, P-7, and P-9 are present in Gram- Plasmid maintenance. An active partitioning system is negative bacteria (25, 74, 75, 78), although many others, commonly found in these Inc group plasmids, with ParA, a including plasmids from Gram-positive bacteria, probably Walker-type ATPase, ParB, a DNA-binding protein, parS, a belong to unidentified Inc groups (74, 78). In this review, ParB-binding centromere-like site (for detail, please see we focus on the degradative plasmids in Inc groups in recent review by Funnell and Slavcev (35)). The par systems Pseudomonas, because the basic features of three plasmid of IncP-1 and IncP-9 are closely related at the protein level, groups (excluding IncP-2) under laboratory conditions have but the IncP-7 par system is quite distinct (108). The been well-characterized (see below). First, the basic features ParA and ParB homologues in the IncP-1 system are IncC brought about by the plasmid backbone of three Inc groups in and KorB (1). The most likely candidate for the parS site Pseudomonas are summarized and then their behavior in a of IncP-1 plasmids is located downstream of korB (35). variety of microcosms is described. IncP-1 plasmids have been considered stable in most hosts, however; De Gelder and coworkers (22) found hosts in which Basic features of IncP-1, IncP-7 and IncP-9 plasmids the plasmid was not stable, although why remains unclear. IncP-9 plasmids also have this system (parABkorAparC is Host range of plasmids. Host range is particularly impor- located on oriV-rep upstream), although detailed functional tant when considering the behavior of degradative plasmids analyses have not been reported. Intriguingly, the oriV-rep in natural environments and microcosms. The hosts of the system of IncP-9 cannot function in E. coli unless it is degradative plasmids in the IncP-1, IncP-7 and IncP-9 accompanied by at least part of the par region in cis (88). As groups are listed in Table 1, as determined by the identifica- for the IncP-7 plasmids, products of parWAB are essential tion of isolated degrading bacteria, transconjugants obtained for their maintenance, although the parS site has not been by mating assays with single recipients, or transconjugants determined; and the function of ParW is still unclear (92). from environmental samples after inoculation of the plasmid Plasmid transfer. The conjugative transfer of a plasmid is host cells. The definition of the host range of plasmids initiated by the cleavage of DNA in the origin of transfer remains controversial. “Broad host range” plasmids have (oriT) by a protein named relaxase that covalently binds to been proposed to be able to replicate themselves and be the oriT region. Afterward, the DNA-relaxase complex is maintained stably without any selections in at least two transported into the recipient cell by an export system, the different subdivisions of Proteobacteria (108). According type IV secretion system. These events are regulated by to this definition, IncP-1 plasmids have a broad host range, two systems: Mating Pair Formation (Mpf) and DNA and IncP-7 plasmids a narrow host range (Table 1). As for Transfer and Replication (Dtr). Additionally, a coupling the IncP-9 plasmids, there are several reports that this group protein, associated with the cell membrane, actively pumps is found in β-Proteobacteria (Table 1), though their stability the DNA into the recipient cell (33). A plasmid that carries without selection markers was not been assessed. In this all the gene sets needed for its conjugative transfer is called review, we recognize the IncP-9 plasmids as having an “self-transmissible”. Small plasmids only carry the gene set ‘intermediate’ host range. Because the host ranges of
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