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.2013 Nov;9(11):e1003891.
doi: 10.1371/journal.pgen.1003891. Epub 2013 Nov 7.

Molecular recognition by a polymorphic cell surface receptor governs cooperative behaviors in bacteria

Affiliations

Molecular recognition by a polymorphic cell surface receptor governs cooperative behaviors in bacteria

Darshankumar T Pathak et al. PLoS Genet.2013 Nov.

Abstract

Cell-cell recognition is a fundamental process that allows cells to coordinate multicellular behaviors. Some microbes, such as myxobacteria, build multicellular fruiting bodies from free-living cells. However, how bacterial cells recognize each other by contact is poorly understood. Here we show that myxobacteria engage in recognition through interactions between TraA cell surface receptors, which leads to the fusion and exchange of outer membrane (OM) components. OM exchange is shown to be selective among 17 environmental isolates, as exchange partners parsed into five major recognition groups. TraA is the determinant of molecular specificity because: (i) exchange partners correlated with sequence conservation within its polymorphic PA14-like domain and (ii) traA allele replacements predictably changed partner specificity. Swapping traA alleles also reprogrammed social interactions among strains, including the regulation of motility and conferred immunity from inter-strain killing. We suggest that TraA helps guide the transition of single cells into a coherent bacterial community, by a proposed mechanism that is analogous to mitochondrial fusion and fission cycling that mixes contents to establish a homogenous population. In evolutionary terms, traA functions as a rare greenbeard gene that recognizes others that bear the same allele to confer beneficial treatment.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. OM exchange is strain specific.
A) Schematic for how OM exchange was scored. Donor cell OMs were labeled with either lipophilic or lipo (SSOM)-mCherry red fluorescent reporters. Transfer was determined by the ability of labeled green fluorescent recipient cells to turn red. B) Assessment of 16 independentM. xanthus isolates and a closely relatedM. fulvus species for their ability to exchange OM components. Distinct recognition groups are color coded. Donors and recipients indicate the direction of transfer. T, transfer; minus (−), no transfer; ±, poor transfer. Strain mixtures that were not tested are indicated as blank boxes.
Figure 2
Figure 2. The TraA PA14-like domain is polymorphic and correlates to recognition groupings.
A) TraA amino acid (AA) variation derived from a sequence alignment from 16M. xanthus strains is plotted.M. fulvus represents a distinct species and was excluded. Black rectangles in the hyper-variable region represent indels that range from one to seven codons in length. The signal sequence (SS) and a putative protein sorting tag (MYXO-CTERM) are also labeled. B) Phylogenetic tree derived from the PA14 polymorphic region, unrooted. Node support values are given as posterior probabilities. The multiple-sequence alignment used to generate the tree is provided in Figure S1. Recognition groups are boxed and labeled. A dashed border indicates the heterogeneous recognition group. C) Domain similarity between three TraA sequences is graphically depicted and color coded. Gray and blue regions contain divergent sequences. Transfer compatibility of TraA variants is shown by green arrows (transfer) or red bars (no transfer). Specificity was determined by PA14 domain relatedness. The apparent chimeric domain architecture, depicting sequence relatedness, suggests that DNA rearrangements occurred between ancestraltraA alleles. See Figure S2 for alignments.
Figure 3
Figure 3. TraA is a cell surface receptor.
A) Western blot with TraA-PA14 antibodies against whole-cell lysates fromtraA+ (DW1463) and ΔtraA (DW1467) strains. Molecular weight markers (kDa) are shown at the left, and the arrow indicates the TraA-specific band at ∼100 kDa. B) TraA immunofluorescence micrographs of live non-permeabilized cells. The same strains and primary antibodies were used as in A. White bar represents 2 µm.
Figure 4
Figure 4. TraA is the molecular determinant for specificity.
Schematic representations of cell-cell interactions are shown on the left, in which variant TraA receptors are color coded. On the right are merged micrographs from red and green fluorescence images after mixed cells were collected from an agar surface. The laboratoryM. xanthus strain was labeled with a red lipophilic DiD membrane dye, which does not transfer to theM. fulvus cells, which were labeled with the green fluorescent tracer dye. In contrast, an isogenicM. xanthus traA allele replacement strain (DW1470), which encodes thetraAM. fulvus allele, enables recognition and transfer withM. fulvus (yellow/orange cells).
Figure 5
Figure 5.traA allele–specific interactions in extracellular complementation of gliding motility.
Protein transfer was assayed by the ability of nonmotile recipient mutants (ΔcglC Δtgl) to be complemented extracellularly by a nonmotile, nonstimulatable donor that encodes the wild-type CglC and Tgl proteins –. The four engineered donor strains encoded the indicatedtraA allele replacements. The recipient strains were merodiploid with the indicatedtraA alleles and the originaltraADK1622 allele. Strains were mixed at a 1∶1 cell ratio, and micrographs were taken after 1 day. Images with black borders showtraA allele combinations that restore motility, which occurs by protein transfer . Strains are listed in Table S1.
Figure 6
Figure 6.traA allele–specific regulation of swarming.
Indicated motile strains were mixed with isogenic engineered nonmotile laboratory strains that encoded the indicatedtraA alleles. Mixtures in which both strains encoded identicaltraA alleles or belonged to the same recognition group are highlighted with a black border, and they all exhibited swarm inhibition. A nonmotile ΔtraA strain (DW1467) was used as a negative control (full swarming). Stereomicrographs were taken after 2 days of incubation. Assay was done as described .
Figure 7
Figure 7. TraA-dependent OM exchange confers protection from inter-strain killing.
A) LabeledM. fulvus (stained red with DiD lipid dye) was mixed at a 1∶1 cell ratio with isogenic labeled DK1622 derivative strains (stained green with CFDA SE) that contain either TraADK1622 (DK8601*) or TraAM. fulvus (DW1470*). After incubation on an agar surface for the indicated times, cells were collected for microscopic examination to determine the ratio of red to green or yellow cells. Between 300 and >1,000 cells were scored for each time point. B) The experiment was carried out as in A, except DK801 was mixed with isogenic DK1622 derivative strains that contained either TraADK1622 (DK8601*) or ΔTraA (DW1467*). Results are representative from multiple experiments.
Figure 8
Figure 8. Schematic overview for how TraA-mediated cell-cell interactions can contribute toward myxobacterial social behaviors.
Cell genotypes and TraA receptors are color coded to indicate genetic relatedness. Related TraA receptors bind through proposed homophilic interactions. Populations of low genetic diversity would likely result in only sibling interactions, whereas diverse populations could result in non-kin interactions and could contribute toward group selection dynamics . Subsequent OM fusion and component exchange results in the indicated social outcomes. The ability of non-kin cells to interact could result in positive fitness outcomes. For example, if two distinctM. xanthus populations are of insufficient size to build a fruiting body, their combined populations, as mediated by TraA interactions, may be able to surmount this barrier.
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