No full-text available
To read the full-text of this research,
you can request a copy directly from the author.
Studies on the free-living generations of Strongyloides planiceps, 1943 II. Effect of temperature on the developmental types
Abstract
In order to study the effect of temperature on the developmental course of S. planiceps, cultures (241-320 eggs in 0.2 g of feces) were held at various temperatures between 12 and 36 C. At high temperature 28-36 C, many free living females with a few infective larvae were formed. At low temperatures, 12-16 C, free living females became few in number, and conversely many infective larvae were formed. Thus the temperature was proved as one of the factors which concerned the determination of developmental course eitherp65l11w1=It to free living females or to infective larvae. On the other hand, free living males were formed always in a constant ratio irrespective of temperature, and thought to be genetically determined. The question when the course to free living females or infective larvae will be determined, was studied experimentally at various temperatures. It became evident that the future developmental course of the early first stage larvae of about 220-280 μ long were not determined yet, but they were susceptible to environmental conditions. The developmental course of larvae of about 300-350 μ long, which were at the stage of first molting, was already fixed. Therefore, the course to free living females or infective larvae was considered to be determined in the first stage larvae.
... For S. stercoralis post-parasitic female larvae, temperatures below 34°C promote indirect development, while temperatures greater than 34°C promote development directly to L3i [42,43]. However, the opposite trend is observed for S. ratti, S. planiceps, and S. papillosus, where direct development is favored at 13-15°C and indirect development favored at 30°C or above [44][45][46]. Provided food is abundant and the population density is low, culture temperature does not appear to affect the proportion of P. trichosuri larvae developing to L3i, which include both males and females for this genus [47,48]. ...
Parasitic nematodes inflict a vast global disease burden in humans as well as animals and plants of agricultural importance; understanding how these worms infect their hosts has significant health and economic implications. In humans, soil-transmitted parasitic nematodes cause hookworm disease and strongyloidiasis, and vector-transmitted parasitic nematodes cause filariasis. The infectious form of the species causing these diseases is a developmentally arrested third-stage larva (L3i). Molecular mechanisms governing L3i developmental arrest and activation within a host have been poorly understood. An analogous developmentally arrested third-stage larva—the dauer larva—forms during stressful environmental conditions in the free-living nematode Caenorhabditis elegans and is controlled by four cellular signaling pathways. The "dauer hypothesis" posits that similar mechanisms regulate dauer and L3i development. The parasitic nematode Strongyloides stercoralis was used to test the dauer hypothesis because its life cycle includes both parasitic and free-living forms. To investigate the role of canonical dauer pathway homologs in regulating L3i arrest and activation, this study utilized transcriptome sequencing (RNAseq), transgenesis, and pharmacological studies. Transcripts encoding cyclic guanosine monophosphate (cGMP) pathway components were coordinately up-regulated in L3i. Application of membrane-permeable 8-bromo-cGMP resulted in activation of L3i and modulation of ligand transcripts in other pathways. In comparison to C. elegans, S. stercoralis has few genes encoding insulin/IGF-1 -like signaling (IIS) ligands, several of which have transcripts modulated during L3i development. Application of the phosphatidylinositol-3 kinase inhibitor, LY294002, prevented L3i activation in host-like conditions. The S. stercoralis transcriptome includes seven homologs of the single C. elegans dauer transforming growth factor β (TGFβ) ligand, three of which are only expressed in L3i. Although the C. elegans nuclear hormone receptor ligand delta7-dafachronic acid (DA) stimulates L3i activation, putative DA biosynthetic genes were not coordinately regulated in L3i development. These data demonstrate that S. stercoralis has homologs for nearly every component in the four canonical dauer pathways, that cGMP signaling may transduce host cues during L3i activation, and that IIS regulates L3i arrest and activation. However, dauer TGFβ signaling appears to function in L3i arrest, an opposite role than in C. elegans, and endogenous DA regulation of L3i development remains largely unexplored.
... In these species, either a lower concentration of food or food that has depleted nutritional value due to washing and autoclaving results in a higher proportion of infective larval development. With respect to temperature, it has been found that extremes in culturing conditions (either high or low incubation temperatures) for S. fuelleborni result in a slight increase in homogonic development [55] and that a lower temperature also results in more infective larval development in S. ratti [13,56,57], S. planiceps [58] and S. papillosus [59] . However, the lower incubation temperatures used in the Strongyloides experiments may have had an effect on the growth of bacteria used as the food source, and as such the environmental signal tested may have been as much food availability as temperature. ...
Parasitism is an important life history strategy in many metazoan taxa. This is particularly true of the Phylum Nematoda, in which parasitism has evolved independently at least nine times. The apparent ease with which parasitism has evolved amongst nematodes may, in part, be due to a feature of nematode development acting as a pre-adaptation for the transition from a free-living to a parasitic life history. One candidate pre-adaptive feature for evolution in terrestrial nematodes is the dauer larva, a developmentally arrested morph formed in response to environmental signals.
We investigated the role of dauer development in the nematode, Parastrongyloides trichosuri, which has retained a complete free-living life cycle in addition to a life cycle as a mammalian gastrointestinal parasite. We show that the developmental switch between these life histories is sensitive to the same environmental cues as dauer arrest in free-living nematodes, including sensitivity to a chemical cue produced by the free-living stages. Furthermore, we show that genetic variation for the sensitivity of the cue(s) exists in natural populations of P. trichosuri, such that we derived inbred lines that were largely insensitive to the cue and other lines that were supersensitive to the cue.
For this parasitic clade, and perhaps more widely in the phylum, the evolution of parasitism co-opted the dauer switch of a free-living ancestor. This lends direct support to the hypothesis that the switch to developmental arrest in the dauer larva acted as a pre-adaptation for the evolution of parasitism, and suggests that the sensory transduction machinery downstream of the cue may have been similarly co-opted and modified.
Classical and reverse genetics remain invaluable tools for the scientific investigation of model organisms. Genetic analysis of endoparasites is generally difficult because the sexual adults required for crossing and other manipulations are usually hidden within their host.
Strongyloides
spp. and
Parastrongyloides
spp. are notable exceptions to this and their free-living adults offer unique opportunities to manipulate these parasites experimentally. Here I review the modes of inheritance in the two generations of
Strongyloides
/
Parastrongyloides
and I discuss the opportunities and the limitations of the currently available methodology for the genetic analysis of these two genera.
SUMMARY Strongyloides venezuelensis is a parasitic nematode that infects rodents. Although Strongyloides species described to date are known to exhibit parthenogenetic reproduction in the parasitic stage of their life cycle and sexual reproduction in the free-living stage, we did not observe any free-living males in S. venezuelensis in our strain, suggesting that the nematode is likely to depend on parthenogenetic reproduction. We confirmed by cytological analysis that S. venezuelensis produces eggs by parthenogenesis during the parasitic stage of its life cycle. Phylogenetic analysis using nearly the full length of 18S and D3 region of 28S ribosomal RNA gene suggested that S. venezuelensis is distantly related to another rodent parasite, namely Strongyloides ratti, but more closely related to a ruminant parasite, Strongyloides papillosus. Karyotype analysis revealed S. venezuelensis reproduces with mitotic parthenogenesis, and has the same number of chromosomes as S. papillosus (2n = 4), but differs from S. ratti (2n = 6) in this regard. These results, taken together, suggest that S. venezuelensis evolved its parasitism for rodents independently from S. ratti and, therefore, is likely to have a different reproductive strategy.
It is well known that the Strongyloides species have two different developmental courses-direct and indirect development-and selection of these courses is affected by various environmental factors. This study examined the effect of temperature on the development of first-stage larvae (L1s) of Strongyloides ratti, to clarify how larvae adapt and survive at unsuitable temperatures. It was revealed that L1s cultured at 4 or 10 °C for 120 h could not develop because of growth arrest or delay. However, L1s could develop after transfer to culture at 25 °C for 48 h. Although larvae cultured at 25 °C take indirect development, larvae subjected to low-temperature stimulation (at 4 or 10 °C) take direct development into infective third-stage larvae (L3s), and only 1 min of low-temperature stimulation was sufficient to induce direct development. Morphological study of low-temperature-stimulated L3s revealed that those stimulated at 4 °C (L3-4) showed less development, but those stimulated at 10 °C (L3-10) developed as well as the control (no low-temperature stimulation). Furthermore, we revealed that L3-10 showed similar infectivity to the control when they were injected subcutaneously into rats as the final host, which indicated that L3-10 grew normally. We conclude that S. ratti has a survival strategy of growth arrest or delay if excreted in cold conditions. Moreover, even if they start development after transfer to suitable conditions, they memorize low-temperature stimulation, which leads them to direct development thereafter so that they can immediately infect the final host.
The present work gives a brief review on the major aspects of the effect of constant and changing temperatures on the development of stronglid nematode eggs. The effect of culture media on the range of temperatures at which the eggs may hatch as well as the rate of their hatching is also included. In addition, a revision of resistance of the eggs to low and high temperatures is also tackled.
The present research investigated the influence of temperature and time of larvae culture on the infectivity of Strongyloides venezuelensis. Mice were infected s.c. with 1500 larvae of S. venezuelensis maintained at 28 °C for three days of culture (dc), 28 °C for seven dc or 18 °C for seven dc. On days 1, 3, 5, 7, 14 and 21 post-infection the animals were sacrificed and cell numbers in the blood, peritoneal cavity fluid (PCF), broncoalveolar fluid (BALF), cytokines, immunoglobulins, number of parasites and eggs/g of feces were quantified. Results demonstrated an increase in eosinophils and mononuclear cells in the blood, PCF and BALF of infected mice. Larvae at 28 °C/3dc induced earlier eosinophils in the PCF and BALF as opposed to larvae at 28 °C/7dc and 18 °C/7dc. Larvae at 28 °C/7dc induced higher synthesis of IL-4, IL-5 and IL-10 on days 5 and 7 post-infection. Larvae at 28 °C/3dc in culture induced higher synthesis of IL-12 than larvae of seven dc, but time in culture induced better synthesis of IFN-γ after larval migration had ceased and only adult worms were present. Larvae at 28 °C/3dc in culture induced higher synthesis of IgG and IgG1 and expelled less female parasites than larvae cultivated for seven days. In conclusion, it was observed that the infectivity of S. venezuelensis is influenced by variations in temperature and time of culture.
The effect of fatty acids was studied on the developmental direction of Strongyloides ratti first-stage larvae (L1). The proportion of third-stage infective larvae increased markedly when L1 were cultured in faeces with added fatty acids such as palmitic (C16), stearic (C18), oleic (C18:1) and linoleic (C18:2) acids. Unsaturated fatty acids were more effective than saturated ones. Moreover, the proportion of infective larvae increased with quantity of linoleic acid but the triacylglycerols of any fatty acid had no effect. These results suggest that these free fatty acids cause physiological changes that determine the developmental course of L1 of S. ratti in nature.
The effects of duration of infection and of temperature and nourishment in cultures on development of free-living generations of Strongyloides stercoralis were studied quantitatively. Rhabditiform larvae, 228-353 microns long, were collected from infected dogs with or without prednisolone treatment using the Baermann apparatus. Cultures were carried out by the filter paper test-tube method under the following condition: incubation temperature 15-40 degrees C and faecal dilution 1:0-1:16. Rhabditiform larvae developed predominantly to free-living females at incubation temperatures of 15-30 degrees C and low faecal dilutions, but filariform larvae appeared mainly under extreme conditions such as high temperature. Recovery rates of filariform larvae were inversely related to those of females. It was remarkable that high temperature, but not low faecal dilution, affected development of filariform larvae. Although the appearance of free-living males was constant in various environmental conditions, the present study indicated an increase in free-living males with the duration of infection. Thus, it seems that free-living males are already fixed as male in the egg stage, and potential female rhabditiform larvae differentiate into free-living females or filariform larvae depending on environmental factors. There is no marked difference in the development of rhabditiform larvae into filariform larvae in either the immunosuppressed dog or the intact dog.
A forkhead transcription factor gene, fktf-1, which we propose to be orthologous to the Caenorhabditis elegans dauer-regulatory gene daf-16 has been discovered in the parasitic nematode Strongyloides stercoralis. Genomic and cDNA sequences from both species predict alternately spliced a and b message isoforms. In contrast to C. elegans, where two a isoforms, daf-16a1 and daf-16a2, are found, a single fktf-1a isoform is found in S. stercoralis. Five of the 10 introns found in the C. elegans gene are found in the proposed S. stercoralis ortholog. Functional motifs common to DAF-16 and several mammalian forkhead transcription factors are conserved in FKTF-1. These include the forkhead DNA binding domain, four Akt/protein kinase B phosphorylation sites and a C-terminal domain that may associate with factors such as the steroid receptor coactivator and other factors necessary for transcriptional regulation. An N-terminal serine-rich domain found in DAF-16A is greatly expanded in FKTF-1A. This domain is missing in DAF-16B, FKTF-1B and all mammalian orthologs. FKTF-1 shows the closest phylogenetic relationship to DAF-16 among all known mammalian and nematode forkhead transcription factors. Like its proposed Caenorhabditis ortholog, the fktf-1 message is expressed at all stages of the life cycle examined thus far. Discovery of fktf-1 indicates the presence of an insulin-like signalling pathway in S. stercoralis similar to that known to regulate dauer development in C. elegans. This pathway is a likely candidate to control infective larval arrest and reactivation as well as regulation of the switch between parasitic and free-living development in the parasite.
In the genus Strongyloides, larval development external to the host is known to be markedly affected by a variety of environmental factors. This investigation focuses on the effect of temperature on Strongyloides ratti. Low temperature (15 degrees C) was shown to favor direct development, producing infective larvae, while high temperature (25 degrees C) favored indirect development, producing free-living females and males. Different courses of development were brought about by either a 16-h temperature stimulus at 15 degrees C or a 6-h temperature stimulus at 25 degrees C. Moreover, eggs were not susceptible to the cold-temperature stimulus of 15 degrees C, while newly hatched larvae were. The results indicate that the developmental course of S. ratti larvae external to the host is determined at a relatively early stage before the first molt.
ResearchGate has not been able to resolve any references for this publication.