scholarly journals A Novel Glycolipid Biosurfactant Confers Grazing Resistance upon Pantoea ananatis BRT175 against the Social Amoeba Dictyostelium discoideum

mSphere ◽  
2016 ◽  
Vol 1 (1) ◽  
Author(s):  
Derek D. N. Smith ◽  
Arvin Nickzad ◽  
Eric Déziel ◽  
John Stavrinides

ABSTRACT The genetic factors used for host interaction by the opportunistic human pathogen Pantoea ananatis are largely unknown. We identified two genes that are important for the production of a biosurfactant that confers grazing resistance against the social amoeba Dictyostelium discoideum. We show that the biosurfactant, which exhibits cytotoxicity toward the amoebae, is a glycolipid that incorporates a hexose rather than rhamnose. The production of this biosurfactant may confer a competitive advantage in the environment and could potentially contribute to the establishment of opportunistic infections. Pantoea is a versatile genus of bacteria with both plant- and animal-pathogenic strains, some of which have been suggested to cause human infections. There is, however, limited knowledge on the potential determinants used for host association and pathogenesis in animal systems. In this study, we used the model host Dictyostelium discoideum to show that isolates of Pantoea ananatis exhibit differential grazing susceptibility, with some being resistant to grazing by the amoebae. We carried out a high-throughput genetic screen of one grazing-resistant isolate, P. ananatis BRT175, using the D. discoideum pathosystem to identify genes responsible for the resistance phenotype. Among the 26 candidate genes involved in grazing resistance, we identified rhlA and rhlB, which we show are involved in the biosynthesis of a biosurfactant that enables swarming motility in P. ananatis BRT175. Using liquid chromatography-mass spectrometry (LC-MS), the biosurfactant was shown to be a glycolipid with monohexose-C10-C10 as the primary congener. We show that this novel glycolipid biosurfactant is cytotoxic to the amoebae and is capable of compromising cellular integrity, leading to cell lysis. The production of this biosurfactant may be important for bacterial survival in the environment and could contribute to the establishment of opportunistic infections. IMPORTANCE The genetic factors used for host interaction by the opportunistic human pathogen Pantoea ananatis are largely unknown. We identified two genes that are important for the production of a biosurfactant that confers grazing resistance against the social amoeba Dictyostelium discoideum. We show that the biosurfactant, which exhibits cytotoxicity toward the amoebae, is a glycolipid that incorporates a hexose rather than rhamnose. The production of this biosurfactant may confer a competitive advantage in the environment and could potentially contribute to the establishment of opportunistic infections.

mSphere ◽  
2019 ◽  
Vol 4 (3) ◽  
Author(s):  
Stephanie Santarriaga ◽  
Alicia Fikejs ◽  
Jamie Scaglione ◽  
K. Matthew Scaglione

ABSTRACTThe social amoebaDictyostelium discoideum’s proteome contains a vast array of simple sequence repeats, providing a unique model to investigate proteostasis. Upon conditions of cellular stress,D. discoideumundergoes a developmental process, transitioning from a unicellular amoeba to a multicellular fruiting body. Little is known about how proteostasis is maintained duringD. discoideum’s developmental process. Here, we have identified a novel α-crystallin domain-containing protein, heat shock protein 48 (HSP48), that is upregulated duringD. discoideumdevelopment. HSP48 functions in part by forming a biomolecular condensate via its highly positively charged intrinsically disordered carboxy terminus. In addition to HSP48, the highly negatively charged primordial chaperone polyphosphate is also upregulated duringD. discoideumdevelopment, and polyphosphate functions to stabilize HSP48. Upon germination, levels of both HSP48 and polyphosphate dramatically decrease, consistent with a role for HSP48 and polyphosphate during development. Together, our data demonstrate that HSP48 is strongly induced duringDictyostelium discoideumdevelopment. We also demonstrate that HSP48 forms a biomolecular condensate and that polyphosphate is necessary to stabilize the HSP48 biomolecular condensate.IMPORTANCEDuring cellular stress, many microbes undergo a transition to a dormant state. This includes the social amoebaDictyostelium discoideumthat transitions from a unicellular amoeba to a multicellular fruiting body upon starvation. In this work, we identify heat shock protein 48 (HSP48) as a chaperone that is induced during development. We also show that HSP48 forms a biomolecular condensate and is stabilized by polyphosphate. The findings here identifyDictyostelium discoideumas a novel microbe to investigate protein quality control pathways during the transition to dormancy.


2012 ◽  
Vol 11 (5) ◽  
pp. 638-644 ◽  
Author(s):  
Yoshinori Araki ◽  
Hideki D. Shimizu ◽  
Kentaro Saeki ◽  
Marina Okamoto ◽  
Lixy Yamada ◽  
...  

ABSTRACT Sexual reproduction is essential for the maintenance of species in a wide variety of multicellular organisms, and even unicellular organisms that normally proliferate asexually possess a sexual cycle because of its contribution to increased genetic diversity. Information concerning the molecules involved in fertilization is accumulating for many species of the metazoan, plant, and fungal lineages, and the evolutionary consideration of sexual reproduction systems is now an interesting issue. Macrocyst formation in the social amoeba Dictyostelium discoideum is a sexual process in which cells become sexually mature under dark and submerged conditions and fuse with complementary mating-type cells. In the present study, we isolated D. discoideum insertional mutants defective in sexual cell fusion and identified the relevant gene, macA , which encodes a highly glycosylated, 2,041-amino-acid membrane protein (MacA). Although its overall similarity is restricted to proteins of unknown function within dictyostelids, it contains LamGL and discoidin domains, which are implicated in cell adhesion. The growth and development of macA -null mutants were indistinguishable from those of the parental strain. The overexpression of macA using the V18 promoter in a macA -null mutant completely restored its sexual defects. Although the macA gene encoded exactly the same protein in a complementary mating-type strain, it was expressed at a much lower level. These results suggest that MacA is indispensable for gamete interactions in D. discoideum , probably via cell adhesion. There is a possibility that it is controlled in a mating-type-dependent manner.


PLoS ONE ◽  
2012 ◽  
Vol 7 (9) ◽  
pp. e46150 ◽  
Author(s):  
Clea Scala ◽  
Xiangjun Tian ◽  
Natasha J. Mehdiabadi ◽  
Margaret H. Smith ◽  
Gerda Saxer ◽  
...  

Microbiology ◽  
2021 ◽  
Author(s):  
Catherine J. Pears ◽  
Julian D. Gross

The social amoeba Dictyostelium discoideum is a versatile organism that is unusual in alternating between single-celled and multi-celled forms. It possesses highly-developed systems for cell motility and chemotaxis, phagocytosis, and developmental pattern formation. As a soil amoeba growing on microorganisms, it is exposed to many potential pathogens; it thus provides fruitful ways of investigating host-pathogen interactions and is emerging as an influential model for biomedical research.


2021 ◽  
Vol 22 (1) ◽  
Author(s):  
Simon Yuan Wang ◽  
Elizabeth Ann Pollina ◽  
I-Hao Wang ◽  
Lindsay Kristina Pino ◽  
Henry L. Bushnell ◽  
...  

Abstract Background The evolution of multicellularity is a critical event that remains incompletely understood. We use the social amoeba, Dictyostelium discoideum, one of the rare organisms that readily transits back and forth between both unicellular and multicellular stages, to examine the role of epigenetics in regulating multicellularity. Results While transitioning to multicellular states, patterns of H3K4 methylation and H3K27 acetylation significantly change. By combining transcriptomics, epigenomics, chromatin accessibility, and orthologous gene analyses with other unicellular and multicellular organisms, we identify 52 conserved genes, which are specifically accessible and expressed during multicellular states. We validated that four of these genes, including the H3K27 deacetylase hdaD, are necessary and that an SMC-like gene, smcl1, is sufficient for multicellularity in Dictyostelium. Conclusions These results highlight the importance of epigenetics in reorganizing chromatin architecture to facilitate multicellularity in Dictyostelium discoideum and raise exciting possibilities about the role of epigenetics in the evolution of multicellularity more broadly.


2019 ◽  
Vol 63 (8-9-10) ◽  
pp. 343-357
Author(s):  
Adam Kuspa ◽  
Gad Shaulsky

William Farnsworth Loomis studied the social amoeba Dictyostelium discoideum for more than fifty years as a professor of biology at the University of California, San Diego, USA. This biographical reflection describes Dr. Loomis’ major scientific contributions to the field within a career arc that spanned the early days of molecular biology up to the present day where the acquisition of high-dimensional datasets drive research. Dr. Loomis explored the genetic control of social amoeba development, delineated mechanisms of cell differentiation, and significantly advanced genetic and genomic technology for the field. The details of Dr. Loomis’ multifaceted career are drawn from his published work, from an autobiographical essay that he wrote near the end of his career and from extensive conversations between him and the two authors, many of which took place on the deck of his beachfront home in Del Mar, California.


Cells ◽  
2017 ◽  
Vol 6 (3) ◽  
pp. 18 ◽  
Author(s):  
Eunice Domínguez-Martín ◽  
Elena Cardenal-Muñoz ◽  
Jason King ◽  
Thierry Soldati ◽  
Roberto Coria ◽  
...  

2019 ◽  
Vol 63 (8-9-10) ◽  
pp. 371-382
Author(s):  
James M. Medina ◽  
P.M. Shreenidhi ◽  
Tyler J. Larsen ◽  
David C. Queller ◽  
Joan E. Strassmann

The social amoeba Dictyostelium discoideum has provided considerable insight into the evolution of cooperation and conflict. Under starvation, D. discoideum amoebas cooperate to form a fruiting body comprised of hardy spores atop a stalk. The stalk development is altruistic because stalk cells die to aid spore dispersal. The high relatedness of cells in fruiting bodies in nature implies that this altruism often benefits relatives. However, since the fruiting body forms through aggregation there is potential for non-relatives to join the aggregate and create conflict over spore and stalk fates. Cheating is common in chimeras of social amoebas, where one genotype often takes advantage of the other and makes more spores. This social conflict is a significant force in nature as indicated by rapid rates of adaptive evolution in genes involved in cheating and its resistance. However, cheating can be prevented by high relatedness, allorecognition via tgr genes, pleiotropy and evolved resistance. Future avenues for the study of cooperation and conflict in D. discoideum include the sexual cycle as well as the relationship between D. discoideum and its bacterial symbionts. D. discoideum’s tractability in the laboratory as well as its uncommon mode of aggregative multicellularity have established it as a promising model for future studies of cooperation and conflict.


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