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© A. Renz and A. Streit/MPI for Developmental Biology, Tübingen

The parasitic Nematode Group

Project leader:
Adrian Streit

Department:
IV - Evolutionary Biology

Director:
Ralf. J. Sommer

Office:
Kostadinka Krause
Spemannstrasse 39
D-72076 Tübingen
Germany
Phone: +49 7071 601 403/441
Fax: +49 7071 601 498

Group members:

Group pictures

Alumni:

  • Anna Dyka (Bachelor student 5/2012 - 3/2013)
  • Alexander Eberhardt (Diploma and PhD student 9/2005 - 1/2010) 
  • Li Guo (PhD student 10/2008 - 2/2016, including interruption for family reasons)
  • Julia Hildebrandt (Diploma and PhD student 9/2009 - 6/2014)
  • Tegegn Jaleta (PhD student 6/2012 - 12/2016
  • Stephan Knierer (PhD student 1/2005 - 1/2010)
  • Arpita Kulkarni (PhD student 1/2010 - 9/2015)
  • Ryuji Minasaki (PhD student 4/2003 - 9/2007)
  • Linda Nemetschke (PhD student 5/2006 - 7/2010)
  • Viktoria Wegewitz (tech. ass. and PhD student 4/2003 - 11/2009)
  • Olga Zhukova (PhD student 1/2010 - 1/2014)

Projects

Strongyloides spp. a parasitic nematode with a facultative free-living generation

The nematode genus Strongyloides consists of parasites that live as parthenogenetic females in the small intestines of their vertebrate hosts. In addition to producing parasitic offspring, Strongyloides spp. can also form a facultative free-living generation with males and females. A generalized life cycle of Strongyloides sp. is shown in Figure 1. For a general introduction into the biology of Strongyloides sp. by Mark E. Viney and James B. Lok click here. We work mainly with S. papillosus, a common parasite of sheep and goats, which can be raised in rabbits and with S. ratti, a parasite of rats. We also maintain free living cultures of Parastrongyloides trichosuri, a closely related facultative parasite of Australian possums. Work on P. trichosuri is conduct in collaboration with Warwick Grant from La Trobe University at Melbourne.

Figure 1: Left: Life cycle of Strongyloides papillosus (from Nemetschke et al., 2010). Right: DIC micrographs of parasitic (top, photo: L. Nemetschke) and free-living (bottom) S. papillosus adults (from Streit, 2008).

Genetics

Classical genetic approaches are rarely used with metazoan endo-parasites, largely because the adult stages are usually hidden within hosts, making controlled crosses difficult. The existence of a free-living generation in Strongyloides spp. offers a remarkable opportunity for the experimental manipulation of a parasite. We would like to explore this opportunity and conduct genetic screens in Strongyloides spp. We established a genetic linkage map for S. ratti (in collaboration with Mark Viney, University of Bristol, Nemetschke et al. 2010) and we established a protocol for chemical mutagenesis of S. ratti (Guo et al. 2015). We are analyzing and comparing the inheritance and linkage of molecular genetic markers in S. ratti and in S. papillosus. We are particularly interested in differences between the two species, which relate to their different sex determining systems.

Sex determination and sex chromosomes

The sex determining mechanisms vary within the genus Strongyloides. There are species with true sex chromosomes such that individuals with two X chromosomes (plus two pairs of autosomes) are female and individuals with one X are male. Other species, for example S. papillosus have only two pairs of chromosomes, one of which is considerably larger than the other. Already more tan 30 years ago it was speculated that this is the result of a fusion of the X chromosome with one of the autosomes. In old, cytological studies some authors found no chromosomal differences between the sexes of S. papillosus. Others described that in males a portion of one chromosome is eliminated, thereby creating a hemizygous region (sex specific chromatin diminution). Recently, by combining cytological and molecular genetic approaches, we demonstrated that in S. papillosus males an internal portion of one of the two larger chromosomes is eliminated. Further we showed that the region undergoing chromatin diminution contains a high number of genes and is homologous to the X chromosome of S. ratti. The portions of the longer chromosome that is not diminished corresponds to chromosome number I of S. ratti (Nemetschke et al. 2010). These findings, in combination with comparative studies we performed in collaboration with Warwick Grant (La Trobe University) on the sister taxon Parastrongyloides trichosuri, strongly support the chromosome fusion hypothesis (Kulkarni et al. 2013). 

Interestingly, all larvae produced by the free-living generation are female and become infective. We attempt to understand, how this is achieved. We were able to show that in S. papillosus genetically male determining mature sperm never forms (Nemetschke, 2010; Kulkarni, 2016). Surprisingly, in S. ratti null-X sperm and also very early embryos with a male karyotype appear to exist but the male embryos may be unviable (Kulkarni, 2016)

People involved in this project:

Present:

  • Alex Dulovic
  • Dorothee Harbecke
  • Anja Holz
  • Siyu Zhou

Past:

  • Anna Dyka
  • Alexander Eberhardt
  • Li Guo
  • Tegegn Jaleta
  • Arpita Kulkarni
  • Linda Nemetschke
  • Olga Zhukova

Strongyloides stercoralis in humans and dogs - to what extent are dogs a source for human Strongyloidiasis

Strongyloidiasis, a human disease caused by mainly Strongyloides stercoralis, is a neglected tropical disease. It is however, not limited to tropical regions. It is known that S. stercoralis can also infect dogs. Therefore, there is a potential for transmission of S. stercoralis between humans and dogs. However, it is still a matter of debate to what extent Strongyloidiasis is a zoonotic disease. Recently we initiated a project comparing S. stercoralis from humans and dogs using molecular genetic and genomic approaches. For this project we collaborate with the group of Peter Odermatt at the Swiss Tropical and Publich Health Institute at Basel and with Virak Khieu and Sinuon Muth from the Cambodian National Center for Parasitology, Entomology and Malaria Control at Phnom Penh.

People involved in this project:

Present:

  • Siyu Zhou

Past:

  • Li Guo
  • Tegegn Jaleta

Population biology of the filarial nematode Onchocerca ochengi, a bovine parasite closely related to the causing agent of river blindness

The filarial nematode Onchocerca ochengi is a parasite of cattle in tropical regions. It is closely related with O. volvulus that causes human onchocerciasis, commonly known as river blindness. The two species of Onchocerca share the insect intermediate host Simulium damnosum. Reproducing adult females of O. ochengi live in nodules in the skin of their host. Males, which are much smaller than the females, are present in the nodules at an average number of about one male per nodule. The young first stage juveniles, called microfilariae, leave the nodule of their mother and wait to be taken up by the intermediate host during a blood meal.

Figure 2: O. ochengi nodules in the skin of a zebu (left), and surgically isolated (center). Mature female (right) (Photos: A. Renz).

The topics we are mainly interested in include:

  • Reproductive biology, in particular the relative contribution of different adult individuals to the pool of microfilariae in the skin of the host (see Hildebrandt et al. 2012/2014).
  • The phylogenetic relationship of different O. ochengi populations and closely related bovine and human Onchocerca species (see Hildebrandt et al. 2014; Eisenbarth et al. 2014).

For this project we collaborate closely with Alfons Renz from the University of Tübingen and with the Programme Onchocercoses, a Euro-African research network in Ngoundéré, Cameroon.

People involved in this project:

Present:

  • Siyu Zhou

Past:

  • Li Guo
  • Tegegn Jaleta

Publications

Baskaran, P., Jaleta, T. G., Streit, A. and Rödelsperger, C. (2017). Duplications and positive selection drive the evolution of parasitism-associated gene families in the nematode Strongyloides papillosus. Genome Biology and Evolution, in press.

Streit, A. (2017). Genetics: Modes of Reproduction and Genetic Analysis. Parasitology, in press (Review, special issue on Strongyloides spp.).

Jaleta, T., G., Rödelsperger, C. and Streit, A. (2017). Parasitological and transcriptomic comparison of Strongyloides ratti infections in natural and in suboptimal permissive hosts. Experimental Parasitology, in press (special issue) DOI:10.1016/j.exppara.2016.12.003.

Streit, A. and Davis, R. E. (2016). Chromatin diminution version 2. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net/,  DOI: 10.1002/9780470015902.a0001181.pub2 (Review).

Kulkarni, A., Lightfoot, J. W. and Streit, A. (2016). Germline organization in Strongyloides nematodes reveals alternative differentiation and regulation mechanisms. Chromosoma  125, 725-745.     doi:10.1007/s00412-015-0562-5

Dulovic, A., Puller, V. and Streit, A. (2016) Optimizing culture conditions for free-living stages of the nematode parasite Strongyloides rattiExperimental Parasitology 168, 25-30. 10.1016/j.exppara.2016.06.005.

Streit, A., Wang, J., Kang, Y. and Davis, R. E. (2016). Gene Silencing and Sex Determination by Programmed DNA Elimination in Parasitic Nematodes. Current opinion in Microbiology 32 120-127 (Review).

Hunt, V. L., Tsai, I. J., Coghlan, A., Reid, A. J., Holroyd, N., Foth, B. J., Tracey, A., Cotton, J. A., Stanley, E. J., Beasley, H., Bennett, H., Brooks, K., Harsha, B., Kajitani, R., Kulkarni, A., Harbecke, D., Nagayasu, E., Nichol, S., Ogura, Y., Quail, M., Randle, N., Ribeiro, D., Sanchez-Flores, A., Hayashi, T., Itoh, T., Denver, D. R., Grant, W., Stoltzfus, J. D., Lok, J. B., Murayama, H., Wastling, J., Streit, A., Kikuchi, T., Viney, M. E., Matthew Berriman, M. (2016). The Genomic Basis of Parasitism in the Strongyloides Clade of Nematodes. Nature Genetics  48, 299-307.  doi:10.1038/ng.3495

Kulkarni, A., Holz, A., Rödelsperger, C., Harbecke, D. and Streit, A. (2016). Differential chromatin amplification and chromosome complements in the germline of Strongyloididae (Nematoda). Chromosoma  125, 125-136.  doi:10.1007/s00412-015-0532-y

Guo, L., Chang, Z., Dieterich, C. and Streit, A. (2015). A protocol for chemical mutagenesis in Strongyloides ratti. Experimental Parasitology  158, 2-7 (special issue).   .

Witte, H., Moreno, E., Rödelsperger, C., Kim, J. S., Kim, J. S., Streit, A. and Sommer, R. J. (2015). Gene inactivation using the CRISPR/Cas9 system in the nematode Pristionchus pacificus. Development Genes and Evolution 255, 55-62.

Hildebrandt, J. C., Eisenbarth, A., Renz, A. and Streit, A. (2014). Reproductive biology of Onchocerca ochengi, a nodule forming filarial nematode in zebu cattle. Veterinary Parasitology 205, 318-329.

Streit, A. (2014). How to become a parasite without sex chromosomes: a hypothesis for the evolution of Strogyloides sp. and related nematodes. Parasitology 141, 1244-1254 (Review).

Schär, F., Guo. L., Streit, A., Khieu, V., Sinuon, M., Marti, H and Odermatt, P. (2014). Strongyloides stercoralis genotypes in humans in Cambodia. Parasitology Inernational 63, 533-536.

Kulkarni, A., Dyka, A., Nemetschke, L., Grant, W. N. and Streit, A. (2013). Parastrongyloides trichosuri suggests that XX/XO sex determination is ancestral in Strongyloididae (Nematode). Parasitology 140, 1822-1830.

Rödelsperger, C. and Streit, A. (2013). Komplexität im Kleinen - Nematoden-Genome im Vergleich. BIOspektrum 6/13, 606-610 (in German).

Eisenbarth, A., Ekale, D., Hildebrandt, J. C., Achukwi, M. D, Streit, A. and Renz, A. (2013). Molecular evidence of ‘Siisa form’, a new genotype related to Onchocerca ochengi in cattle from North Cameroon. Acta Tropica 127, 261-265.

Rödelsperger, C., Streit, A. and Sommer, R. J. (2012). Structure, function and evolution of the nematode genome. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net/ DOI: 10.1002/9780470015902.a0024603 (Review).

Streit, A. (2012) Silencing by throwing away: a role for chromatin diminution. Developmental Cell 23, 918-919 (Preview).

Hildebrandt, J. C., Eisenbarth, A., Renz, A. and Streit, A. (2012). Single worm genotyping demonstrates that Onchocerca ochengi females simultaneously produce progeny sired by different males. Parasitology Research 111, 2217-2221.

Sommer R. J. and Streit, A. (2011). Comparative Genetics and Genomics of Nematodes: Genome Structure, Development and Lifestyle. Annual Review of Genetics 45, 1-20 (Review).

Nemetschke, L., Eberhardt, A. G., Hertzberg, H. and Streit, A. (2010). Genetics, chromatin diminution and sex chromosome evolution in the parasitic nematode genus StrongyloidesCurrent Biology 20, 1687-1696.

Streit, A. and Sommer, R. J. (2010). Genetics: Random expression goes binary. Nature 463, 891-892 (News and Views).

Nemetschke, L., Eberhardt, A. G., Viney, M. E. and Streit, A. (2010). A genetic map of the animal-parasitic nematode Strongyloides ratti. Molecular and Biochemical Parasitiology 169, 124-127.

Wegewitz, V., Schulenburg, H. and Streit, A. (2009). Do males facilitate the spread of novel phenotypes within populations of the androdioecious nematode Caenorhabditis elegansJournal of Nematology 41, 247-254.

Minasaki R., Puoti A. and Streit A. (2009). The DEAD-box protein MEL-46 is required in the germ line of the nematode Caenorhabditis elegans. BMC Developmental Biology 9, 35.

Ogawa, A., Streit, A., Antebi, A. and Sommer, R. J. (2009). A conserved endocrine mechanism controls the formation of dauer and infective larvae in nematodes. Current Biology 19, 67-71.
Summary of this article, written for a broad audience (in German). Appeared in the newsletter of the German Society for Parasitology 1/2009.

Eberhardt, A. G., Mayer, W. E., Bonfoh, B. and Streit, A. (2008). The Strongyloides (Nematoda) of sheep and the predominant Strongyloides of cattle form at least two different, genetically isolated populations. Veterinary Parasitology 157, 89-99.

Wegewitz, V., Schulenburg, H. and Streit, A. (2008) Experimental insight into the proximate causes of male persistence variation among two strains of the androdioecious Caenorhabditis elegans (Nematoda). BMC Ecology 8, 12.

Streit, A. (2008). Reproduction in Strongyloides (Nematoda): a life between sex and parthenogenesis. Parasitology 135, 285-294 (Review).

Eberhardt, A. G., Mayer, W. E. and Streit, A. (2007). The free-living generation of the nematode Strongyloides papillosus undergoes sexual reproduction. International Journal for Parasitology 37, 989-1000.

Minasaki, R. and Streit, A. (2007). mel-47, a novel protein required for early cell divisions in the nematode Caenorhabditis elegans. Molecular Genetics and Genomics 277, 315-328.

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