scholarly journals Kin discrimination drives territorial exclusion during Bacillus subtilis swarming and restrains exploitation of surfactin

2021 ◽  
Author(s):  
Barbara Kraigher ◽  
Monika Butolen ◽  
Polonca Stefanic ◽  
Ines Mandic Mulec
Keyword(s):  
Surface Tension ◽  
Bacillus Subtilis ◽  
Public Good ◽  
Competitive Exclusion ◽  
Important Determinant ◽  
Kin Discrimination ◽  
Related Strain ◽  
Initial Ratio ◽  
Surface Colonization ◽  
Positive Frequency

AbstractSwarming is the collective movement of bacteria across a surface. It requires the production of surfactants (public goods) to overcome surface tension and provides an excellent model to investigate bacterial cooperation. Previously, we correlated swarm interaction phenotypes with kin discrimination between B. subtilis soil isolates, by showing that less related strains form boundaries between swarms and highly related strains merge. However, how kin discrimination affects cooperation and territoriality in swarming bacteria remains little explored. Here we show that the pattern of surface colonization by swarming mixtures is influenced by kin types. Closely related strain mixtures colonize the surface in a mixed swarm, while mixtures of less related strains show competitive exclusion as only one strain colonizes the surface. The outcome of nonkin swarm expansion depends on the initial ratio of the competing strains, indicating positive frequency-dependent competition. We find that addition of surfactin (a public good excreted from cells) can complement the swarming defect of nonkin mutants, whereas close encounters in nonkin mixtures lead to territorial exclusion, which limits the exploitation of surfactin by nonkin nonproducers. The work suggests that kin discrimination driven competitive territorial exclusion may be an important determinant for the success of cooperative surface colonization.

scholarly journals Kin discrimination promotes horizontal gene transfer between unrelated strains in Bacillus subtilis

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Polonca Stefanic ◽  
Katarina Belcijan ◽  
Barbara Kraigher ◽  
Rok Kostanjšek ◽  
Joseph Nesme ◽  
...  
Keyword(s):  
Bacillus Subtilis ◽  
Gene Transfer ◽  
Horizontal Gene Transfer ◽  
Social Interactions ◽  
Recipient Strain ◽  
Donor Strain ◽  
Kin Discrimination ◽  
Defence Mechanisms ◽  
Donor Cells ◽  
Novel Alleles

AbstractBacillus subtilis is a soil bacterium that is competent for natural transformation. Genetically distinct B. subtilis swarms form a boundary upon encounter, resulting in killing of one of the strains. This process is mediated by a fast-evolving kin discrimination (KD) system consisting of cellular attack and defence mechanisms. Here, we show that these swarm antagonisms promote transformation-mediated horizontal gene transfer between strains of low relatedness. Gene transfer between interacting non-kin strains is largely unidirectional, from killed cells of the donor strain to surviving cells of the recipient strain. It is associated with activation of a stress response mediated by sigma factor SigW in the donor cells, and induction of competence in the recipient strain. More closely related strains, which in theory would experience more efficient recombination due to increased sequence homology, do not upregulate transformation upon encounter. This result indicates that social interactions can override mechanistic barriers to horizontal gene transfer. We hypothesize that KD-mediated competence in response to the encounter of distinct neighbouring strains could maximize the probability of efficient incorporation of novel alleles and genes that have proved to function in a genomically and ecologically similar context.

scholarly journals Applying modern coexistence theory to priority effects

2019 ◽  
Vol 116 (13) ◽  
pp. 6205-6210 ◽  
Author(s):  
Tess Nahanni Grainger ◽  
Andrew D. Letten ◽  
Benjamin Gilbert ◽  
Tadashi Fukami
Keyword(s):  
Growth Rates ◽  
Competitive Exclusion ◽  
Abiotic Factors ◽  
Priority Effects ◽  
Competitive Interactions ◽  
Competing Species ◽  
Coexistence Theory ◽  
Dependent Growth ◽  
Established Population ◽  
Positive Frequency

Modern coexistence theory is increasingly used to explain how differences between competing species lead to coexistence versus competitive exclusion. Although research testing this theory has focused on deterministic cases of competitive exclusion, in which the same species always wins, mounting evidence suggests that competitive exclusion is often historically contingent, such that whichever species happens to arrive first excludes the other. Coexistence theory predicts that historically contingent exclusion, known as priority effects, will occur when large destabilizing differences (positive frequency-dependent growth rates of competitors), combined with small fitness differences (differences in competitors’ intrinsic growth rates and sensitivity to competition), create conditions under which neither species can invade an established population of its competitor. Here we extend the empirical application of modern coexistence theory to determine the conditions that promote priority effects. We conducted pairwise invasion tests with four strains of nectar-colonizing yeasts to determine how the destabilizing and fitness differences that drive priority effects are altered by two abiotic factors characterizing the nectar environment: sugar concentration and pH. We found that higher sugar concentrations increased the likelihood of priority effects by reducing fitness differences between competing species. In contrast, higher pH did not change the likelihood of priority effects, but instead made competition more neutral by bringing both fitness differences and destabilizing differences closer to zero. This study demonstrates how the empirical partitioning of priority effects into fitness and destabilizing components can elucidate the pathways through which environmental conditions shape competitive interactions.

scholarly journals A Combinatorial Kin Discrimination System in Bacillus subtilis

2016 ◽  
Vol 26 (6) ◽  
pp. 733-742 ◽  
Author(s):  
Nicholas A. Lyons ◽  
Barbara Kraigher ◽  
Polonca Stefanic ◽  
Ines Mandic-Mulec ◽  
Roberto Kolter
Keyword(s):  
Bacillus Subtilis ◽  
Kin Discrimination

scholarly journals An Efficient Producing-Bioemulsifier by Bacillus Subtilis UCP 0146 Isolated from Mangrove Sediments

2018 ◽  
Author(s):  
Patrícia. C.V.S. Maia ◽  
Vanessa P. Santos ◽  
Adriana S Ferreira ◽  
Marcos A.C. Luna ◽  
Thayse A. L. Silva ◽  
...  
Keyword(s):  
Surface Tension ◽  
Bacillus Subtilis ◽  
Engine Oil ◽  
Textile Dye ◽  
Mangrove Sediments ◽  
Ionic Charge ◽  
Emulsification Index ◽  
Charge Stability ◽  
Cassava Wastewater

In this work was investigated the potential of Bacillus subtilis UCP 0146 in the bioconversion of the medium containing 100% of cassava flour wastewater to obtain bioemulsifier. The evaluation of the production was carried out by the emulsification index (IE24) and surface tension (TS). The ionic charge, stability (temperature, salinity and pH measured by IE24 and viscosity), ability to remove and disperse oil and textile dye were investigated. B.subtilis produced an anionic bioemulsifier in the medium containing 100% of cassava wastewater in condition 4 of the factorial design (9% of the inoculum, at 35 °C and agitation of 100 rpm) with surface tension of 39mN/m, IE24 of 95.2 % and yield 2.69 g.L-1. Stability at different pH (2-8), temperatures (0-120ºC) and NaCl, dispersed (55.83 cm2-ODA) and reduced the viscosity of the burned engine oil (90.5 cP) , removed 94.4% petroleum and demonstrated efficiency in methylene blue removal (62.2%). The bioemulsifier and its synthesis from bacteria and also emphases on the role of surfactants in oil remediation.

Enhanced Hydrocarbon Biodegradation by a Newly Isolated Bacillus subtilis Strain

2004 ◽  
Vol 59 (3-4) ◽  
pp. 205-208 ◽  
Author(s):  
Nelly Christova ◽  
Borjana Tuleva ◽  
Boryana Nikolova-Damyanova
Keyword(s):  
Surface Tension ◽  
Bacillus Subtilis ◽  
Hydrocarbon Biodegradation ◽  
Subtilis Strain ◽  
Emulsifying Activity ◽  
Hydrophobic Compounds ◽  
High Concentrations ◽  
Rhamnolipid Biosurfactant ◽  
Hydrocarbon Substrates ◽  
Soluble Substrate

The relation between hydrocarbon degradation and biosurfactant (rhamnolipid) production by a new Bacillus subtilis 22BN strain was investigated. The strain was isolated for its capacity to utilize n-hexadecane and naphthalene and at the same time to produce surfaceactive compound at high concentrations (1.5 -2.0 g l-1). Biosurfactant production was detected by surface tension lowering and emulsifying activity. The strain is a good degrader of both hydrocarbons used with degradability of 98.3 ± 1% and 75 ± 2% for n-hexadecane and naphthalene, respectively. Measurement of cell hydrophobicity showed that the combination of slightly soluble substrate and rhamnolipid developed higher hydrophobicity correlated with increased utilization of both hydrocarbon substrates. To our knowledge, this is the first report of Bacillus subtilis strain that degrades hydrophobic compounds and at the same time produces rhamnolipid biosurfactant.

scholarly journals Kin discrimination between sympatric Bacillus subtilis isolates

2015 ◽  
Vol 112 (45) ◽  
pp. 14042-14047 ◽  
Author(s):  
Polonca Stefanic ◽  
Barbara Kraigher ◽  
Nicholas Anthony Lyons ◽  
Roberto Kolter ◽  
Ines Mandic-Mulec
Keyword(s):  
Bacillus Subtilis ◽  
Cooperative Behavior ◽  
Potential Effect ◽  
Differential Treatment ◽  
Plant Roots ◽  
Strongly Correlated ◽  
Ecological Interactions ◽  
Kin Discrimination ◽  
Phylogenetic Relatedness ◽  
History Of

Kin discrimination, broadly defined as differential treatment of conspecifics according to their relatedness, could help biological systems direct cooperative behavior toward their relatives. Here we investigated the ability of the soil bacterium Bacillus subtilis to discriminate kin from nonkin in the context of swarming, a cooperative multicellular behavior. We tested a collection of sympatric conspecifics from soil in pairwise combinations and found that despite their history of coexistence, the vast majority formed distinct boundaries when the swarms met. Some swarms did merge, and most interestingly, this behavior was only seen in the most highly related strain pairs. Overall the swarm interaction phenotype strongly correlated with phylogenetic relatedness, indicative of kin discrimination. Using a subset of strains, we examined cocolonization patterns on plant roots. Pairs of kin strains were able to cocolonize roots and formed a mixed-strain biofilm. In contrast, inoculating roots with pairs of nonkin strains resulted in biofilms consisting primarily of one strain, suggestive of an antagonistic interaction among nonkin strains. This study firmly establishes kin discrimination in a bacterial multicellular setting and suggests its potential effect on ecological interactions.

scholarly journals Water surface tension modulates the swarming mechanics of Bacillus subtilis

2015 ◽  
Vol 6 ◽  
Author(s):  
Wan-Ju Ke ◽  
Yi-Huang Hsueh ◽  
Yu-Chieh Cheng ◽  
Chih-Ching Wu ◽  
Shih-Tung Liu
Keyword(s):  
Surface Tension ◽  
Bacillus Subtilis ◽  
Water Surface

scholarly journals Genetic Requirements for Potassium Ion-Dependent Colony Spreading in Bacillus subtilis

2005 ◽  
Vol 187 (24) ◽  
pp. 8462-8469 ◽  
Author(s):  
Rebecca F. Kinsinger ◽  
Daniel B. Kearns ◽  
Marina Hale ◽  
Ray Fall
Keyword(s):  
Bacillus Subtilis ◽  
Ph Control ◽  
Growth Conditions ◽  
Gene Replacement ◽  
Potassium Ion ◽  
Nucleotide Biosynthesis ◽  
Surface Colonization ◽  
Transposon Insertion ◽  
Colony Spreading ◽  
Sliding Motility

ABSTRACT Undomesticated strains of Bacillus subtilis exhibit extensive colony spreading on certain soft agarose media: first the formation of dendritic clusters of cells, followed by spreading (pellicle-like) growth to cover the entire surface. These phases of colonization are dependent on the level of potassium ion (K+) but independent of flagella, as verified with a mutant with a hag gene replacement; this latter finding highlights the importance of sliding motility in colony spreading. Exploring the K+ requirement, directed mutagenesis of the higher-affinity K+ transporter KtrAB, but not the lower-affinity transporter KtrCD, was found to inhibit surface colonization unless sufficient KCl was added. To identify other genes involved in K+-dependent colony spreading, transposon insertion mutants in wild-type strain 3610 were screened. Disruption of genes for pyrimidine (pyrB) or purine (purD, purF, purH, purL, purM) biosynthetic pathways abolished the K+-dependent spreading phase. Consistent with a requirement for functional nucleic acid biosynthesis, disruption of purine synthesis with the folic acid antagonist sulfamethoxazole also inhibited spreading. Other transposon insertions disrupted acetoin biosynthesis (the alsS gene), acidifying the growth medium, glutamine synthetase (the glnA gene), and two surfactin biosynthetic genes (srfAA, srfAB). This work identified four classes of surface colonization mutants with defective (i) potassium transport, (ii) surfactin formation, (iii) growth rate or yield, or (iv) pH control. Overall, the ability of B. subtilis to colonize surfaces by spreading is highly dependent on balanced nucleotide biosynthesis and nutrient assimilation, which require sufficient K+ ions, as well as growth conditions that promote sliding motility.

scholarly journals Interactions between Streptomyces coelicolor and Bacillus subtilis: Role of Surfactants in Raising Aerial Structures

2006 ◽  
Vol 188 (13) ◽  
pp. 4918-4925 ◽  
Author(s):  
Paul D. Straight ◽  
Joanne M. Willey ◽  
Roberto Kolter
Keyword(s):  
Surface Tension ◽  
Bacillus Subtilis ◽  
Streptomyces Coelicolor ◽  
Antagonistic Activity ◽  
Positive Role ◽  
Amphipathic Peptide ◽  
Major Barrier ◽  
Altered Expression ◽  
Aerial Growth ◽  
Aerial Hyphae

ABSTRACT Using mixed-species cultures, we have undertaken a study of interactions between two common spore-forming soil bacteria, Bacillus subtilis and Streptomyces coelicolor. Our experiments demonstrate that the development of aerial hyphae and spores by S. coelicolor is inhibited by surfactin, a lipopeptide surfactant produced by B. subtilis. Current models of aerial development by sporulating bacteria and fungi postulate a role for surfactants in reducing surface tension at air-liquid interfaces, thereby removing the major barrier to aerial growth. S. coelicolor produces SapB, an amphipathic peptide that is surface active and required for aerial growth on certain media. Loss of aerial hyphae in developmental mutants can be rescued by addition of purified SapB. While a surfactant from a fungus can substitute for SapB in a mutant that lacks aerial hyphae, not all surfactants have this effect. We show that surfactin is required for formation of aerial structures on the surface of B. subtilis colonies. However, in contrast to this positive role, our experiments reveal that surfactin acts antagonistically by arresting S. coelicolor aerial development and causing altered expression of developmental genes. Our observations support the idea that surfactants function specifically for a given organism regardless of their shared ability to reduce surface tension. Production of surfactants with antagonistic activity could provide a powerful competitive advantage during surface colonization and in competition for resources.

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