Putative Attachment Factors Described for Epiphytic Bacteria and Plant Pathogens
Type of bacteria Attachment factor(s)a Ref. Nitrogen-fixing
Rhizobium japonicum EPS 49
Bradyrhizobium japonicum BJ38 lectin (Gal/Lac) 52
Rhizobium trifolii CPS 25
Rhizobium leguminosarum Rhicadhesin 21, 26
Rhizobium leguminosarum bv. trifolii LPS 50
Rhizobium leguminosarum bv. trifolii RapA1c 53
Rhizobium meliloti (Sinorhizobium) Nex18 187
Agrobacterium tumefaciens LPS 64
Agrobacterium tumefaciens T-pilus, F-conjugation factor 188
Agrobacterium tumefaciens Rhicadhesin 21
Agrobacterium tumefaciens att-encoded proteins 60
Agrobacterium tumefaciens CPS 61
Erwinia carotovora Type 1 fimbriae, Hrp 88, 188
Erwinia chrysanthemi Hrp proteins 188, 189
Erwinia chrysanthemi HecA (FHA) 85
Klebsiella aerogenes Type 3 fimbriae 111,188
Pantoea stewartii Hrp 188
Pseudomonas aeruginosad Type IV pili 104
Pseudomonas aeruginosa PA-IIL lectin6 190
Pseudomonas aeruginosa Type II pseudopilus 81
Pseudomonas fluorescens Type III? 95
Pseudomonas fluorescens Type IVB pili, Hrp 188
Pseudomonas syringae pathovars Type IVB pili, Hrp 188, 191, 192
Ralstonia solanacearum Type IVB pili, Hrp 79,188
Ralstonia solanacearum FHA homologsf 80
Ralstonia solanacearum RSL and RS-IIL lectinsg 83
Xanthomonas campestris Type IVB pili, Hrp 105, 188
Xanthomonas campestris pathovars FHA homologs 106
Xylella axonopodis Flagellum, type IV pili 193
Xylella fastidiosa Type IVB pili? 188
Xylella fastidiosa FHA homologs 194
Azospirillum spp. EPS and CPS 108
Azospirillum brasilense Flagellum (polar) 78, 109
Azospirillum brasilense MOMP 110
Pseudomonas fluorescens Fimbriae 195
Pseudomonas fluorescens Flagella 97
Pseudomonas putida Agglutinin? 99
a EPS, exopolysaccharide; CPS, capsular polysaccharide; LPS, lipopolysaccharide; Hrp, hypersensitive response and pathogenicity; HecA, homologous to FHA; FHA, filamentous hemagglutinin. b Gal, galactose; Lac, lactose.
c Secreted from bacteria and binds to carbohydrate on bacteria. d P. aeruginosa can be both a human and a facultative plant pathogen. e PA-IIL has high affinity for L-fucose.
f FHA, filamentous hemagglutinin; based on gene homologs in different pathovars. g RSL has affinity for L-fucose > L-galactose > L-arabinose/D-fructose/D-mannose; RS-IIL has high affinity for fructose and mannose.
endosymbionts involved in nodule formation and nitrogen fixation on roots provides the most advanced model of plant-microbe interactions. Research continues on understanding the fundamental steps involved . It involves specificity between Gram-negative Rhsp and the host , including the site on roots where it is initiated . The early steps of the process do not involve attachment; chemical signals are released from the plant, inducing bacterial genes that encode the release of corresponding signals to the plant that induce nodule development on roots. Rhsp then adhere tightly to the surface of the curling tips of root hair cells [21,42].
The general consensus model that describes Rhsp root attachment proceeds in two steps (Figure 2.1) . Chemicals released by the plant (e.g., flavonoids) induce movement of bacteria by chemotaxis towards chemicals exuding from the root (Figure 2.1D) ; this results in close contact between the roots and the bacteria and initiation of attachment [21,43]. The first step in attachment involves a bacterial Ca2+-binding protein called rhicadhesin (^14,000 Da) which is responsible for attachment of mostly single (not aggregated, Figure 2.1C) bacterial cells directly to the root hair (Table 2.1) . Growth of the bacteria under low Ca2+ conditions decreases direct attachment considerably , possibly due to the release of rhicadhesin under low Ca2+ . The second step in attachment involves bacterial synthesis of cellulose fibrils that bind rhicadhesin leading to auto-aggregation, and/or firm binding of other bacteria at the site of infection . Under carbon-limitation, R. leguminosarum bv viciae cells form aggregates on root hair tips by attaching to other rhizobia cells (Figure 2.1I and J).
Rhicadhesin inhibits the attachment of many Rhizobiaceae spp. to pea root hair tips, including R. leguminosarum biovars, R. meliloti, R. lupini, Bradyrhizobium japonicum, as well as Agrobacterium tumefaciens (Agt) and A. rhizogenes, indicating that rhicadhesin or rhicadhesin homologs are part of a common mechanism of attachment to root hairs . When Mn2+ concentration is limiting, the bacterial cells attach and form aggregates also, but apparently this process is accelerated by a pea plant lectin that binds to a carbohydrate receptor/ligand on the bacteria (Figure 2.1J) . Transgenic alfalfa plants transformed with pea lectin, bound B. japonicum, and R. leguminosarum better than did untransformed lines . Expression of rhizobium exopolysaccharide (EPS) has been reported to be essential for infection thread entry into the root hairs, possibly due to lectin-carbohydrate interactions . Earlier studies reported that EPS, and not lipopolysac-charide (LPS), was the probable bacterial receptor responsible for specific interactions between R. japonicum cells and soybean root hairs by means of a soybean lectin (Figure 2.1J-2) [48,49].
LPS and lipooligosaccharides (LOS) are potential attachment factors as receptors for lectins expressed by the plant host, since they are prominent cell-surface glycoconjugates in Gram-negative bacteria. Plant-microbe studies indicate that EPS and LPS/LOS both are possible receptors for plant lectins, and can be highly variable within a population of cells depending on the environment and mechanism of gene expression. In two studies, LPS of R. leguminosarum was abundant on cells during their attachment to the rhizoplane of Zea mays compared to cells present in the root cortex ; a 38,000 Mr cell surface lectin in B. japonicum (BJ38), inhibitable by lactose and galactose, also was identified [51,52]. Thus, these separate results define a candidate bacterial carbohydrate receptor and a bacterial lectin (possibly pili) that are involved putatively in attachment to plant lectins (Table 2.1) , or plant carbohydrates (Table 2.1 and Figure 2.1J), respectively [51,52].
In an attempt to clone the rhicadhesin gene of R. leguminosarum bv. trifolii, a unipolar cell surface protein, RapA1, was identified that bound to cognate carbohydrates on the bacteria . The RapA1 protein was proposed to be a bacterial lectin. The unipolar location of the lectin and activity in agglutination/aggregation of bacteria indicated it is similar to the B. japonicum BJ38 lectin described above (Table 2.1). In an earlier study, polar attachment of R. trifolii by the clover root hair lectin trifolin A to bacterial extracellular microfibrils composed of capsular polysaccharide (CPS) was described . Thus, it is speculated that these bacterial lectins are capable of recognizing carbohydrate structures present both on the bacteria and plant root hairs , a binding activity that could result in both aggregation of bacteria and attachment of bacteria (possibly singly or as aggregates) to root hairs (Figure 2.1I and J). The expression of RapA1 was stable at any growth phase, but the expression of the bacterial receptors was highest during exponential phase of growth, corresponding to higher agglutination . These results reflect the dynamic state of the rhizobial cell surface, which changes due to growth phase and contact with plants, and affects attachment.
2.4.2 Agrobacterium tumefaciens (Agt)
Agt is a Gram-negative bacterium that when inoculated on wounded dicotyledonous plant tissue causes crown gall tumors by transferring a portion (T-DNA) of a resident plasmid (Ti-plasmid) into the plant . The essential nature of Agt attachment to plant wound tissue for Agt root transformation in a pinto bean leaf model was first reported by Lippincott and Lippincott . Subsequent studies have identified multiple Agt mutants or strains defective in attachment to different plant tissues [56-63], although for many of the mutants the functions of the predicted proteins have not been identified or characterized.
Whatley et al. reported that both LPS on Agt cells and purified LPS inhibited specifically Agt tumorigenic activity on pinto bean leaves by >50% . Although specific genes or gene products were not identified, the authors suggested that LPS interacts with the sites of attachment on the leaves.
Five Agt Tn5 transposon mutant strains unable to attach to carrot cells in suspension (107 bacteria/105 cells), and non-tumorigenic on carrot disks and wounded bean leaves, were identified with an associated loss of 33, 34, and 38 kDa proteins . Revertants of the nonattaching mutants were isolated and shown to have regained virulence and ability to attach, confirming the involvement of the proteins in attachment. In addition, LPS purified from the parent and each of the mutant strains, inhibited by 30 to 60% the attachment of Agt to carrot cells, supporting the hypothesis that LPS plays a role also in attachment . Agt biovar 3 (A. vitis), which is predominantly isolated from grapes and causes root decay, produces a polygalacturonase, that appears to function by modifying specifically grape root cells in a manner that increases attachment of the biovar 3 Agt .
In attachment (att) mutants characterized by Matthysse et al. , open reading frames (ORFs) were identified that have homology to genes encoding the membrane-spanning proteins of periplasmic binding protein-dependent (ABC) transporter systems and ATP-binding proteins of Gram-negative bacteria, and to an ORF in an operon of Campylobacter jejuni associated with attachment. These results do not identify a specific attachment factor; rather they suggest other mechanisms involved in attachment, including secretion in or out of cells of a substance required to condition the medium for bacterial attachment, or ATP-transporter-dependent transfer of plant signals into bacteria with induction of a substance important for attachment. One of the attachment mutants was mutated in a gene, attR, homologous to bacterial transacetylase genes . The attR mutant strain lacked an acety-lated CPS present in the parent strain Agt C58, and consequently did not attach to wound sites and was avirulent for legumes and nonlegumes . The attR mutant strain also did not attach to root hairs and root epidermis of nonlegumes, but did attach to these areas on legumes (alfalfa, bean, pea). These results suggested that attR plays a role in binding of Agt to, and in colonization of, root hairs on nonlegume plants, but that attR has no role in colonization of root hairs on legume plants . Thus, two systems for Agt attachment and colonization are available and may function depending on the plant species.
A polysaccharide purified from the water-soluble fraction of a phenol-water extraction of Agt strain C58 cells inhibited the attachment of Agt to carrot cells. The extracted polysaccharide was acidic, acetylated, and composed of glucose, glucosamine, and an unidentified deoxy-sugar . Interestingly, the ligand in carrot cells that binds the Agt polysaccharide may be a homolog of vitronectin (S protein), a serum-spreading factor in animals and part of the extracellular matrix . The vitronectin-like protein was detected immunochemically as present on the surface of carrot cells , and was detected previously on tomatoes, soybeans, and broad beans . If Agt is bound to plant cell vitronectin, and vitronectin is linked by integrin to actin in the cytoskeletal network as it is in animal cells, this would provide an intimate contact for initiation of the crucial step of transport of Agt T-DNA and proteins to the nucleus of plant cells .
Rhicadhesin, noted above as a proteinaceous attachment factor for R. leguminosarum (Table 2.1), was reported to be important in attachment of Agt to pea root hair tips . However, attachment by rhicadhesin in this system was dependent upon sufficient expression in Agt of cyclic p-1,2-glucan, an osmoregulating molecule synthesized by the chvB encoded protein .
Although there are several Agt virulence proteins suspected of interacting with proteins on different plants , a strong candidate for having a role in attachment of Agt to plants is a pilus, the structure of which in Agt is composed predominantly of multiple copies of the VirB2 protein (propilin) [69,70]. The mature pilus is expressed as ~10 nm diameter filaments on the cell surface and is required for transformation, presumably, by interacting with plant cell wall or membrane molecules . This conjugative T-pilus has significant sequence homology to the conjugative F-pilus of E. coli . Mutants produced in Arabidopsis thaliana by T-DNA insertion revealed plant lines resistant to Agt transformation (rat) and modified in Agt attachment to root hairs: rat1, which encodes an arabinogalactan-related enzyme, and rat3, which encodes putatively a plant cell wall protein . Therefore, both carbohydrate and proteins of the plant are implicated as receptors for Agt pili.
Previous to these descriptions of the mechanisms of attachment of Agt to plant cells and their role in transformation, Matthysse et al. described the synthesis of cellulose fibrils by Agt induced by the attachment of the bacteria to carrot cells . Although the cellulose fibrils appeared not to be necessary for initial attachment, they were shown to be important in anchoring Agt and associated bacteria to the plant cell surface, and enmeshing Agt in aggregates associated with tumor formation [71,72]. An 11 kb region (celABCDE) was identified containing two operons involved in cellulose synthesis . Thus, cellulose is important in establishing a stable and perhaps more complex interaction of Agt with plant tissue subsequent to attachment.
2.4.3 Ralstonia (Pseudomonas)solanacearum (Rs) 184.108.40.206 EPS and LPS
Rs is a Gram-negative soilborne plant pathogen (PP) that infects more than 200 species of plants including fresh produce-related plants like tomato, potato, eggplant, banana, and papaya, and causes bacterial wilt disease . Rs enters the root tissue and invades the plant through the xylem, then moves through the vascular system into the aerial parts of the plant (Figure 2.1K). EPS and LPS were identified as major cell surface molecules associated with virulence of Rs, perhaps functioning by blocking the xylem vessel and preventing water movement . Sugars identified in composition analyses of EPS include different proportions of N-acetylgalactosamine, glucose, rhamnose, basillosamine, and uronic acids . At least one Rs LPS O-antigen was characterized chemically and reported to contain rhamnose, N-acetylglucosamine, and xylose . Mutations in Rs EPS genes (ops gene cluster) modified unexpectedly the synthesis of both EPS and LPS, and corresponded to a significant decrease in the ability of Rs to attach to (presumably), and to infect, two-week-old axenic eggplant seedlings (inoculated in cotyledon) and three-week-old eggplant plants (inoculated in leaf stem). Although five of seven complemented ops mutants had nearly their full virulence restored, no association of LPS or EPS with attachment to the plant tissue was defined .
220.127.116.11 Type III Secretion System (T3SS)
Many of the Gram-negative bacterial plant and animal pathogens described in this chapter produce a T3SS, which has been shown in multiple systems to be crucial to the delivery of multiple virulence factors into the extracellular milieu, but more importantly, directly into plant and/or animal cells. The T3SS was discovered by characterization of gene clusters present in pathogenicity islands and in large plasmids with similarities to flagellar assembly genes . The common genes and functions of the T3SS in plants and details regarding the assembly of pilin and avirulence (avr) genes are provided in an excellent review .
The T3SS in plant pathogenic bacteria involve the hrp (hypersensitive reaction and pathogenicity) genes . hrp-related genes that are relevant to attachment of bacteria to plants include those involved in the synthesis of the novel Hrp pilus. The potential role of the Hrp pilus in delivery of bacterial proteins into plant cells by direct interaction suggests that it also is an attachment factor for other plant pathogens and human pathogens with T3SS (e.g., Pseudomonas, Erwinia, Xanthomonas, Ralstonia, Salmonella, Shigella, Yersinia). However, experiments with Rs in a tobacco plant cell co-culture model indicated that T3SS-encoded pili, composed mainly of HrpY protein, had no role in attachment . An interesting finding was the observation of the HrpY pili and fimbriae concentrated at the same end of the Rs cells, perhaps indicating that a unipolar location was important biologically, possibly in attachment with plants other than tobacco. However, in another study, Rs mutants lacking Hrp pili retained twitching motility and, by electron microscopy, a different polarly located pili structure was observed . This Rs pilus is a 17 kDa protein encoded by pilA, and 46% identical to P. aeruginosa type IV pilin. Rs type IV pili were shown in this study to have a role in autoaggregation, biofilm formation on plastic surfaces, and transformation. However, a PilA mutant retained capability to bind to tobacco cells and to tomato roots, but in a nonpolar fashion, indicating that
PilA has a qualitative role in attachment . The lack of a quantitative effect on attachment of Rs lacking either Hrp pili (type III) or type IV pili to tobacco or tomato plant cells/roots indicates that their major role may be more relevant in natural plant environments (e.g., nutrient acquisition, genetic exchange, and movement and biofilm formation in xylem).
18.104.22.168 Type II Secretion System (T2SS)
Multiple T2SS loci have been identified also in the genome sequence of Rs strain GMI1000 . In P. aeruginosa, the T2SS produces bundled fibrils called type II pseudopilins that increase adherence of the bacteria to plastic surfaces and are involved in production of biofilms . The Rs and other species T2SS-encoded fibrils may have a role in attachment to plants.
22.214.171.124 Rs Lectins, Fimbriae, FHA
Two Rs protein lectins with potential roles in attachment have been characterized recently: RSL (9.9 kDa subunit) with activity/specificity for L-fucose > L-galactose > D-arabinose; and RS-IIL (11.6 kDa subunit) with activity/specificity for D-fructose and D-mannose [82,83]. The RS-IIL is similar, but not identical, to the PA-IIL lectin described for P. aeruginosa. The activity of the RS-IIL lectin for sugars also prominent in plant cell walls has stimulated studies of the role of Rs lectins in attachment to more relevant and complex plant glycoconjugates .
Finally, multiple ORFs identified in the Rs genome strain GMI1000 are similar to nonfimbrial adhesins or hemagglutinin (e.g., FHA) molecules, some of which promote strong adhesion to mammalian cells [80,84]. Future work is necessary to determine whether these proteins have any role in attachment of Rs to plants in a complex soil environment.
The soft-rot pathogen Erwinia chrysanthemi (Echr) expresses an adhesin (HecA) that has homology to filamentous hemagglutinins (FHA) expressed in both plant and animal pathogens (Table 2.1) [85,86]. A hecA mutant of Echr had decreased virulence in seedlings of a particular tobacco cultivar, but not other cultivars or plants, indicating a relatively specific attachment . Observation of green fluorescent protein (GFP)-labeled mutant and wild-type strains by confocal microscopy illustrated that the mutant cells did not aggregate by end-to-end attachment, nor attach to seedling roots, nearly as well as the wild-type cells. Attachment of the mutant strain to the leaf surface was decreased dramatically and no Echr aggregates on leaves were observed. Thus, at least with the specific tobacco cultivar described, HecA appears to function as an important Echr adhesin .
Cell suspension cultures of Gypsophila paniculata ("baby's breath'') leaf segments with a pathogenic strain of Erwinia herbicola pv. gypsophilae (Ehg) resulted in a greater than five-fold increase in plant cell aggregation compared to a nonpathogenic Ehg strain, indicating attachment had occurred; electron microscopy revealed intimate attachment by a possible "bridge" between Ehg and the plant surface . However, no attachment molecules related to this interaction were identified.
Both Echr and E. carotovora (Ecar) possess hrp genes encoding a T3SS, but their role in virulence of Ecar had been unclear . Recently, mutations in Hrp system structural genes confirmed that T3SS proteins are required for full virulence of Ecar for potatoes . Erwinia amylovora, the cause of fire blight in many plants, was observed by scanning electron microscopy (SEM) at regions on and in plant leaves, on the epidermis around detachment sites of leaf hairs, and on stems and roots of apple seedlings . Although intimate interactions between the T3SS Hrp pili and Hrp virulence proteins of E. amylovora have been observed by transmission electron microscopy (TEM) , no evidence for direct attachment of the pilus to host cells has been described. Finally, the in vitro specificity of a presumed Erwinia rhapontici (pathogenic for rhubarb) lectin for N-acetyllactosamine (galactose-p1-4N-acetylglucosamine) would be intriguing if it were related to an attachment factor for plants, but it is apparently nonfimbrial, and no attachment factor has been described .
Pseudomonas syringae (Ps) causes disease in more than 80 plant species, including many important produce-related plants . Ps has been studied extensively as both a pathogen and an epiphyte on plant leaves. Attempts to remove epiphytic populations of bacteria on leaves, including Ps, by vigorous washing and sonication revealed that: (1) some bacteria were bound more strongly than others, (2) the phylloplane was heterogeneous relative to optimal attachment/colonization, and (3) pili-minus Ps strains were washed more easily from leaves compared to wild-type Ps [32,93,94].
P. fluorescens (Pf) strains colonize roots and are important competitors for biocontrol of plant pathogens , and also possibly of human pathogens . Flagellin was shown to be important in motility of Pf for chemotaxis and colonization of potato roots . Piliated/fimbriated strains of Pf were shown to bind to roots of corn seedlings better than a nonpiliated variant strain . Fimbriae/pili (34 kDa) purified from Pf strains also bound to the roots. The fibrillar nature of the pili suggests that they may be T2SS pili (see below). Pf hemagglutination activity was inhibited by all sugars representative of those present in plant root exudates, thus indicating carbohydrate-specific binding activity.
Pseudomonas putida (Pp) is common in soil and acts as a plant growth promoter and suppressor of fungal pathogens. A kidney bean root surface glycoprotein was described that agglutinated Pp cells; agglutinationnegative Pp mutants were reported to be 20- to 30-fold less effective in attaching to root surfaces of seedlings . Motility was shown to be associated with efficient Pp attachment to sterile wheat roots in a simplified model system, implicating flagellin as a potential attachment factor . However, no definitive attachment factor was identified for Pp in these two studies.
P. aeruginosa (Pa) provides a good example of a species that can be a nonpathogenic or pathogenic organism in plants and animals [101,102]. This broad pathogenesis for different hosts reflects the conservation of virulence mechanisms for attacking quite different hosts, including possibly mechanisms of attachment . Pa is very relevant also to fundamental studies of the biology of enteric human pathogens in produce; it may provide clues about mechanisms of attachment, communication, and invasion, important for development of methods for minimizing both human and plant pathogens on plants.
The type IV pilus has been described as the most important ''virulence-associated adhesin'' of Pa . However, this is due to the emphasis on characterization of attachment of Pa to specific glycosphingolipids of mammalian epithelial cells. In plant models, differences in Pa attachment to leaves of different arabidopsis ecotypes have been reported . Pa cells were observed attached perpendicularly to, and degrading regions of, the surfaces of leaves; in other regions, cells bound to trichomes in multiple layers probably as biofilms. The perpendicular orientation noted for Pa cells on arabidopsis surfaces is reminiscent of the unipolar location of rhicadhesin, of rhizobium, and of Hrp pili and fimbriae of Rs (described above), and suggests that an attachment factor may be localized similarly. The movement of Pa cells (possibly by type IV pili twitching motility) towards stomatal openings, entry into them, then attachment to host cell walls, reflects pathogenesis similar to erwinia and ralstonia pathogens .
2.4.6 Xanthomonas campestris (Xc)
Type IV-encoded bundle-forming fimbriae have been characterized in Xc pv. vesicatoria (Xcv) . The fimbriae are composed mainly of a protein subunit of 15.5 kDa (FimA). The use of a FimA-mutant strain indicated that fimbriae had no role in colonization of tomato leaves. However, major differences were noted between the wild-type and mutant strains in the amount of cell-cell aggregation in laboratory cultures, on tomato leaf surfaces, and on trichomes, with the wild-type always more prevalent . These results suggest that if the fimbriae assist attachment of Xcv to tomato surfaces, they may be specific for selected regions of the plant, such as trichomes. Putative FHA proteins suspected of being involved in attachment in other species also are present in Xc .
Azospirillum spp. have been investigated because of their nitrogen-fixing capability while in close contact with grass roots . Two different polysaccharide structures were identified in strains of A. brasilense (Abr) and A. lipoferum (Alip): a CPS tightly associated with the cell surface, and an EPS appearing to be less dense and extending from the cell . A wheat lectin, wheat germ agglutinin, bound to Abr and Alip cells, and the binding was inhibited by N-acetylglucosamine. Thus, these results provided evidence of carbohydrate surface structures that are candidate receptors for specific plant lectins .
Abr strains express a polar flagellum . Attachment of a nonmotile Abr flagellar mutant to wheat roots was reduced dramatically, whereas purified flagella bound directly to wheat roots. The major outer membrane protein of Abr was reported to be an adhesin responsible for Abr-Abr aggregation, and the variable attachment of Abr to root extracts of wheat > corn > sorghum > bean >> chickpea > tomato . The degree of aggregation of Abr cells is related possibly to the amount and composition of the EPS and/ or CPS .
Klebsiella spp. are enteric bacteria that can be soilborne, saprophytic, and cause serious human illness. An associative nitrogen-fixing strain of K. aerogenes expressing type 3 fimbriae was characterized for attachment . The fimbriae of 23.5 kDa were associated with hemagglutination of human O erythrocytes, and the adhesion of bacteria to plant seedling roots. In addition, the purified fimbriae also bound directly to root tissue. Other strains of klebsiella also were shown to bind to roots by the type 3 fimbriae . Subsequently, type 1 fimbriae were reported to mediate adherence of K. pneumoniae and Enterobacter agglomerans (Pantoea agglomerans) strains to plant roots, with binding inhibitable by a-methyl-D-mannoside . Thus, different types of fimbriae appeared to mediate adherence of different enteric species to plant roots.
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