Advertisement

Species recognition in social amoebae

  • Ikumi Shibano Hayakawa
  • Kei Inouye
Article
  • 39 Downloads

Abstract

Aggregative multicellularity requires the ability of cells to recognise conspecifics. Social amoebae are among the best studied of such organisms, but the mechanism and evolutionary background of species recognition remained to be investigated. Here we show that heterologous expression of a single Dictyostelium purpureum gene is sufficient for D. discoideum cells to efficiently make chimaeric fruiting bodies with D. purpureum cells. This gene forms a bidirectional pair with another gene on the D. purpureum genome, and they are both highly polymorphic among independent wild isolates of the same mating group that do not form chimaeric fruiting bodies with each other. These paired genes are both structurally similar to D. discoideum tgrB1/C1 pair, which is responsible for clonal discrimination within that species, suggesting that these tgr genes constitute the species recognition system that has attained a level of precision capable of discriminating between clones within a species. Analysis of the available genome sequences of social amoebae revealed that such gene pairs exist only within the clade composed of species that produce precursors of sterile stalk cells (prestalk cells), suggesting concurrent evolution of a precise allorecognition system and a new ‘worker’ cell-type dedicated to transporting and supporting the reproductive cells.

Keywords

Chimaera Dictyostelium purpureum evolution interspecific recognition social amoeba tgr genes 

Notes

Acknowledgements

We would like to thank T. Oyama and M. Ichikawa for their continuous help and encouragement during the course of the study. We also thank P. Schaap and H. Kuwayama for genome sequence data, T. Hayakawa for advice on de novo assembly of NGS data, S. Ito for discussions and help in quantitative PCR, T. Shimada for the use of a qPCR cycler, S. Nonaka, Y. Kamei and Olympus Corporation for use of confocal microscopes in Department of Physics, Y. Yamaguchi for help in interspecies mixing experiments of non-group 4 species, M. M. Hayakawa for insightful comments and suggestions, and V. Nanjundiah for discussions and invaluable comments on the manuscript. Some of the wild isolates were obtained from National BioResource Project Nenkin (http://nenkin.nbrp.jp). This work was supported by Grant-in-Aid for JSPS Fellows 12J01422 to ISH. The DNA sequences for Dp-csaA and Dp-tgrs have been deposited at DDBJ/ENA/GenBank under accession numbers MK002463 to MK002469, for rDNA-ITS of the D. purpureum strains, MK002470 to MK002481, and assembled contigs of the genome of D. purpureum strain P1Ba, RBCH00000000. The strains used in this study can be obtained from National BioResource Project Nenkin (http://nenkin.nbrp.jp).

Supplementary material

12038_2018_9810_MOESM1_ESM.pdf (1.8 mb)
Supplementary material 1 (PDF 1822 kb)

References

  1. Asghar A, Groth M, Siol O, Gaube F, Enzensperger C, Glöckner G and Winckler T 2012 Developmental gene regulation by an ancient intercellular communication system in social amoebae. Protist 163 25–37CrossRefGoogle Scholar
  2. Atzmony D, Zahavi A and Nanjundiah V 1997 Altruistic behaviour in Dictyostelium discoideum explained on the basis of individual selection. Curr. Sci. 72 142–145Google Scholar
  3. Barth A, Müller-Taubenberger A, Taranto P and Gerisch G 1994 Replacement of the phospholipid-anchor in the contact site A glycoprotein of D. discoideum by a transmembrane region does not impede cell adhesion but reduces residence time on the cell surface. J. Cell Biol. 124 205–215CrossRefGoogle Scholar
  4. Benabentos R, Hirose S, Sucgang R, Curk T, Katoh M, Ostrowski EA, Strassmann JE, Queller DC, Zupan B, Shaulsky G and Kuspa A 2009 Polymorphic members of the lag gene family mediate kin discrimination in Dictyostelium. Curr. Biol. 19 567–572CrossRefGoogle Scholar
  5. Benson MR and Mahoney DP 1977 The distribution of dictyostelid slime molds in southern California with taxonomic notes on selected species. Am. J. Bot. 64 496–503CrossRefGoogle Scholar
  6. Beug H, Katz FE and Gerisch G 1973 Dynamics in antigenic membrane sites relating to cell aggregation in Dictyostelium discoideum. J. Cell Biol. 56 647–658CrossRefGoogle Scholar
  7. Bonner JT and Adams MS 1958 Cell mixtures of different species and strains of cellular slime moulds. J. Embryol. Exp. Morphol. 6 346–356PubMedGoogle Scholar
  8. Buchmann K 2014 Evolution of innate immunity: clues from invertebrates via fish to mammals. Front. Immunol. 5 1–8CrossRefGoogle Scholar
  9. Buss LW 1982 Somatic cell parasitism and the evolution of somatic tissue compatibility. Proc. Natl. Acad. Sci. USA 79 5337–5341CrossRefGoogle Scholar
  10. Cavender JC 1973 Geographical distribution of Acrasiae. Mycologia 65 1044–1054CrossRefGoogle Scholar
  11. Cavender JC 1978 Cellular slime molds in tundra forest soils of Alaska including a new species, Dictyostelium septentrionalis. Can. J. Bot. 57 1326–1332CrossRefGoogle Scholar
  12. Cavender JC 2013 A global overview of Dictyostelid ecology with special emphasis in North American forest; in Dictyostelids – evolution, genomics and cell biology (eds) M Romeralo, S Baldauf and R Escalante (Berlin, Heidelberg: Springer-Verlag) pp149–166CrossRefGoogle Scholar
  13. Chen G, Wang J, Xu X, Wu X, Piao R and Siu CH 2013 tgrC1 mediates cell-cell adhesion by interacting with tgrB1 via mutual IPT/TIG domains during development of Dictyostelium discoideum. Biochem. J. 452 259–69CrossRefGoogle Scholar
  14. de Wit RJW and Konijn TM 1983 Identification of the acrasin of Dictyostelium minutum as a derivative of folic acid. Cell Differ. 12 205–210CrossRefGoogle Scholar
  15. Eisenberg RM 1976 Two-dimensional microdistribution of cellular slime molds in forest soil. Ecology 57 380–384.CrossRefGoogle Scholar
  16. Filosa MF 1962 Heterocytosis in cellular slime molds. Am. Naturalist 46 79–92.CrossRefGoogle Scholar
  17. Fiz-Palacios O, Romeralo M, Ahmadzadeh A, Weststrand S, Ahlberg PE and Baldauf S 2013 Did terrestrial diversification of amoebas (amoebozoa) occur in synchrony with land plants? PLoS One 8 e74374CrossRefGoogle Scholar
  18. Gabriel D, Hacker U, Kohler J, Müller-Taubenberger A, Schwartz JM, Westphal M and Gerisch G 1999 The contractile vacuole network of Dictyostelium as a distinct organelle: its dynamics visualized by a GFP marker protein. Correction: 112:U3(1999). J. Cell Sci. 112 3995–4005PubMedGoogle Scholar
  19. Gao EN, Shier P and Siu CH 1992 Purification and partial characterization of a cell adhesion molecule (gp150) involved in postaggregation stage cell-cell binding in Dictyostelium discoideum. J. Biol. Chem. 267 9409–9415PubMedGoogle Scholar
  20. Glöckner G, Lawal HM, Felder M, Singh R, Singer G, Weijer CJ and Schaap P 2016 The multicellularity genes of dictyostelid social amoebae. Nat. Comm. 7 12085CrossRefGoogle Scholar
  21. Gruenheit N, Parkinson K, Stewart B, Howie JA, Wolf JB and Thompson CRL 2017 A polychromatic ‘greenbeard’ locus determines patterns of cooperation in a social amoeba. Nat. Comm. 8 14171CrossRefGoogle Scholar
  22. Hagiwara H, Kawakami S and Hwang JY 2004 Mating system and morphology of the temperate form of Dictyostelium purpureum Olive. Bull. Natl. Sci. Mus. Tokyo, Ser. B 30 71–78Google Scholar
  23. Harada Y, Takagaki Y, Sunagawa M, Saito T, Yamada L, Taniguchi H, Shoguchi E and Sawada H 2008 Mechanism of self-sterility in a hermaphroditic chordate. Science 320 548–550CrossRefGoogle Scholar
  24. Hirose S, Benabentos R, Ho HI, Kuspa A and Shaulsky G 2011 Self-recognition in social amoebae is mediated by allelic pairs of tiger genes. Science 333 467–470CrossRefGoogle Scholar
  25. Hirose S, Chen G, Kuspa A and Shaulsky G 2017 The polymorphic proteins tgrB1 and tgrC1 function as a ligand-receptor pair in Dictyostelium allorecognition. J. Cell Sci. 130 4002–4012CrossRefGoogle Scholar
  26. Jack CN, Ridgeway JG, Mehdiabadi NJ, Jones EI, Edwards TA, Queller DC and Strassmann JE 2008 Segregate or cooperate – a study of the interaction between two species of Dictyostelium. BMC Evol. Biol. 8 293CrossRefGoogle Scholar
  27. Kamboj RK, Gariepy J and Siu CH 1989 Identification of an octapeptide involved in homophilic interaction of the cell adhesion molecule gp80 of Dictyostelium discoideum. Cell 59 615–625CrossRefGoogle Scholar
  28. Katoh K and Standley DM 2013 MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30 772–780.CrossRefGoogle Scholar
  29. Katoh K, Kuma K, Toh H and Miyata T 2005 MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 33 511–518CrossRefGoogle Scholar
  30. Kaushik S and Nanjundiah V 2003 Evolutionary questions raised by cellular slime mold development. Proc. Indian Natl. Sci. Acad. B 69 825–852Google Scholar
  31. Kay RR and Thompson CRL 2001 Cross-induction of cell types in Dictyostelium: evidence that DIF-1 is made by prespore cells. Development 128 4959–4966PubMedGoogle Scholar
  32. Kay RR, Taylor GW, Jermyn KA and Traynor D 1992 Chlorine-containing compounds produced during Dictyostelium development - Detection by labelling with 36Cl. Biochem. J. 281 155–161CrossRefGoogle Scholar
  33. Konijn TM, Barkley DS, Chang YY and Bonner JT 1968 Cyclic AMP: a naturally occurring acrasin in the cellular slime molds. Am. Naturalist 102 225–233CrossRefGoogle Scholar
  34. Korber B. 2000 HIV Signature and Sequence Variation Analysis; in Computational Analysis of HIV Molecular Sequences (eds) AG Rodrigo and GH Learn (Dordrecht, Netherlands: Kluwer Academic Publishers) pp 55–72Google Scholar
  35. Levi S, Polyakov M and Egelhoff TT 2000 Green fluorescent protein and epitope tag fusion vectors for Dictyostelium discoideum. Plasmid 44 231–238CrossRefGoogle Scholar
  36. Litman GW, Cannon JP and Dishaw LJ 2005 Reconstructing immune phylogeny: new perspectives. Nat. Rev. Immunol. 5 866–879CrossRefGoogle Scholar
  37. Mehdiabadi NJ, Jack CN, Farnham TT, Platt TG, Kalla SE, Shaulsky G, Queller DC and Strassmann JE 2006 Kin preference in a social microbe. Nature 442 881–882CrossRefGoogle Scholar
  38. Mehdiabadi NJ, Kronforst MR, Queller DC and Strassmann JE 2009 Phylogeny, reproductive isolation and kin recognition in the social amoeba Dictyostelium purpureum. Evolution 63 542–548CrossRefGoogle Scholar
  39. Nanjundiah V and Sathe S 2011 Social selection and the evolution of cooperative groups: the example of the cellular slime moulds. Integr. Biol. 3, 329–342CrossRefGoogle Scholar
  40. Nei M and Gojobori T 1986 Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 3 418–426PubMedGoogle Scholar
  41. Nydam ML and De Tomaso AW 2011 Creation and maintenance of variation in allorecognition loci: molecular analysis in various model systems. Front. Immunol. 2 79PubMedPubMedCentralGoogle Scholar
  42. Okegawa Y and Motohashi K 2015 A simple and ultra-low cost homemade seamless ligation cloning extract (SLiCE) as an alternative to a commercially available seamless DNA cloning kit. Biochem. Biophys. Rep. 4 148–151PubMedPubMedCentralGoogle Scholar
  43. Ostrowski EA, Katoh M, Shaulsky G, Queller DC and Strassmann JE 2008 Kin discrimination increases with genetic distance in a social amoeba. PLoS Biol. 6 e287CrossRefGoogle Scholar
  44. Parikh A, Miranda ER, Katoh-Kurasawa M, Fuller D, Rot G, Zagar L, Curk T, Sucgang R, Chen R, Zupan B, Loomis WF, Kuspa A and Shaulsky G 2010 Conserved developmental transcriptomes in evolutionarily divergent species. Genome Biol. 11 R35CrossRefGoogle Scholar
  45. Raper KB and Thom C 1941 Interspecific mixtures in the Dictyosteliaceae. Am. J. Bot. 28 69–78CrossRefGoogle Scholar
  46. Romeralo M, Cavender JC, Landolt JC, Stephenson SL and Baldauf SL 2011 An expanded phylogeny of social amoebas (Dictyostelia) shows increasing diversity and new morphological patterns. BMC Evol Biol. 11 84CrossRefGoogle Scholar
  47. Sakaguchi M, Murakami H and Suzaki T 2001 Involvement of a 40-kDa glycoprotein in food recognition, prey capture, and induction of phagocytosis in the protozoon Actinophrys sol. Protist 152 33–41CrossRefGoogle Scholar
  48. Sathe S, Kaushik S, Lalremruata A, Aggarwal RK, Cavender JC and Nanjundiah V 2010 Genetic heterogeneity in wild isolates of cellular slime mold social groups. Microb. Ecol. 60 137–148CrossRefGoogle Scholar
  49. Sathe S, Khetan N and Nanjundiah V 2013 Interspecies and intraspecies interactions in social amoebae. J. Evol. Biol. 27 349–62CrossRefGoogle Scholar
  50. Schilde C, Skiba A and Schaap P 2014 Evolutionary reconstruction of pattern formation in 98 Dictyostelium species reveals that cell-type specialization by lateral inhibition is a derived trait. EvoDevo 5 34CrossRefGoogle Scholar
  51. Schilde C, Lawal HM, Noegel AA, Eichinger L, Schaap P and Glöckner G 2016 A set of genes conserved in sequence and expression traces back the establishment of multicellularity in social amoebae. BMC Genomics 17 871CrossRefGoogle Scholar
  52. Seike T, Nakamura T and Shimoda C 2015 Molecular coevolution of a sex pheromone and its receptor triggers reproductive isolation in Schizosaccharomyces pombe. Proc. Natl. Acad. Sci. USA 112 4405–4410CrossRefGoogle Scholar
  53. Shaffer BM 1962 The Acrasina. Adv. Morphogenesis 2 109–182CrossRefGoogle Scholar
  54. Shimomura O, Suthers HLB and Bonner JT 1982 Chemical identity of the acrasin of the cellular slime mold Polysphondylium violaceum. Proc. Natl. Acad. Sci. USA 79 7376–7379CrossRefGoogle Scholar
  55. Shin SH, Kim S, Kim JY, Lee SJ, Um YS, Oh MK, Kim YR, Lee JW and Yang KS 2012 Complete genome sequence of Enterobacter aerogenes KCTC 2190. J. Bacteriol. 194 2373–2374CrossRefGoogle Scholar
  56. Siu CH, Cho A and Choi HC 1987 The contact site a glycoprotein mediates cell-cell adhesion by homophilic binding in Dictyostelium discoideum. J. Cell Biol. 105 2523–2533CrossRefGoogle Scholar
  57. Stamatakis A. 2014 RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30 1312–1313CrossRefGoogle Scholar
  58. Strassmann JE, Zhu Y and Queller DC 2000 Altruism and social cheating in the social amoeba Dictyostelium discoideum. Nature 408 965–967CrossRefGoogle Scholar
  59. Strassmann JE and Queller DC 2011 Evolution of cooperation and control of cheating in a social microbe. Proc. Natl. Acad. Sci. USA. 108 10855–10862CrossRefGoogle Scholar
  60. Sucgang R, Kuo A, Tian X, Salerno W, Parikh A, Feasley CL, Dalin E, Tu H, et al. 2011 Comparative genomics of the social amoebae Dictyostelium discoideum and Dictyostelium purpureum. Genome Biol. 12 R20CrossRefGoogle Scholar
  61. Swanson AR, Vadell EM and Cavender JC 1999 Global distribution of forest soil dictyostelids. J. Biogeography 26 133–148CrossRefGoogle Scholar
  62. Takuno S, Fujimoto R, Sugimura T, Sato K, Okamoto S, Zhang SL and Nishio T 2007 Effects of recombination on hitchhiking diversity in the Brassica self-incompatibility locus complex. Genetics 177 949–958CrossRefGoogle Scholar
  63. Thompson CRL and Kay RR 2000 The role of DIF-1 signaling in Dictyostelium development. Mol. Cell 6 1509–1514CrossRefGoogle Scholar
  64. Uchinomiya K and Iwasa Y 2013 ‘Evolution of stalk/spore ratio in a social amoeba: cell-to-cell interaction via a signaling chemical shaped by cheating risk. J. Theor. Biol. 336 110–118CrossRefGoogle Scholar
  65. van Es S, Hodgkinson S, Schaap P and Kay RR 1995 Metabolic pathways for differentiation-inducing factor-1 and their regulation are conserved between closely related Dictyostelium species, but not between distant members of the family. Differentiation 58 95–100CrossRefGoogle Scholar
  66. van Haastert PJM, de Wit RJW, Grijpma Y and Konijn TM 1982 Identification of a pterin as the acrasin of the cellular slime mold Dictyostelium lacteum. Proc. Natl. Acad. Sci. USA 79 6270–6274CrossRefGoogle Scholar
  67. Wang J, Hou LS, Awrey D, Loomis WF, Firtel RA and Siu CH 2000 The membrane glycoprotein gp150 is encoded by the lagC gene and mediates cell-cell adhesion by heterophilic binding during Dictyostelium development. Dev. Biol. 227 734–745CrossRefGoogle Scholar
  68. Wang Y and Shaulsky G 2015 TgrC1 has distinct functions in Dictyostelium development and allorecognition. PLoS One 10 e0124270CrossRefGoogle Scholar
  69. Watts DJ and Ashworth JM 1970 Growth of myxamoebae of the cellular slime mould Dictyostelium discoideum in axenic culture. Biochem. J. 119 171–174CrossRefGoogle Scholar
  70. Zerbino DR and Birney E 2008 Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18 821–829CrossRefGoogle Scholar
  71. Zerbino DR, McEwen GK, Margulies EH and Birney E 2009 Pebble and rock band: heuristic resolution of repeats and scaffolding in the velvet short-read de novo assembler. PLoS ONE 4 e8407CrossRefGoogle Scholar

Copyright information

© Indian Academy of Sciences 2018

Authors and Affiliations

  1. 1.Department of Botany, Graduate School of ScienceKyoto UniversityKyotoJapan
  2. 2.Department of Physics, Graduate School of ScienceKyoto UniversityKyotoJapan

Personalised recommendations