scholarly journals Transcriptional variation and divergence of host-finding behaviour in Steinernema carpocapsae infective juveniles

BMC Genomics ◽  
2019 ◽  
Vol 20 (1) ◽  
Author(s):  
Neil D. Warnock ◽  
Deborah Cox ◽  
Ciaran McCoy ◽  
Robert Morris ◽  
Johnathan J. Dalzell
Keyword(s):  
Galleria Mellonella ◽  
Entomopathogenic Nematode ◽  
Gene Families ◽  
Nematode Species ◽  
Host Finding ◽  
Steinernema Carpocapsae ◽  
Differentially Expressed ◽  
Infective Juvenile ◽  
Neuronal Genes ◽  
Sodium Transporter

Abstract Background Steinernema carpocapsae is an entomopathogenic nematode that employs nictation and jumping behaviours to find potential insect hosts. Here we aimed to investigate the transcriptional basis of variant host-finding behaviours in the infective juvenile (IJ) stage of three S. carpocapsae strains (ALL, Breton and UK1), with a focus on neuronal genes known to influence behaviour in other nematode species. Identifying gene expression changes that correlate with variant host-finding behaviours will further our understanding of nematode biology. Results RNA-seq analysis revealed that whilst up to 28% of the S. carpocapsae transcriptome was differentially expressed (P < 0.0001) between strains, remarkably few of the most highly differentially expressed genes (> 2 log2 fold change, P < 0.0001) were from neuronal gene families. S. carpocapsae Breton displays increased chemotaxis toward the laboratory host Galleria mellonella, relative to the other strains. This correlates with the up-regulation of four srsx chemosensory GPCR genes, and a sodium transporter gene, asic-2, relative to both ALL and UK1 strains. The UK1 strain exhibits a decreased nictation phenotype relative to ALL and Breton strains, which correlates with co-ordinate up-regulation of neuropeptide like protein 36 (nlp-36), and down-regulation of an srt family GPCR gene, and a distinct asic-2-like sodium channel paralogue. To further investigate the link between transcriptional regulation and behavioural variation, we sequenced microRNAs across IJs of each strain. We have identified 283 high confidence microRNA genes, yielding 321 predicted mature microRNAs in S. carpocapsae, and find that up to 36% of microRNAs are differentially expressed (P < 0.0001) between strains. Many of the most highly differentially expressed microRNAs (> 2 log2 fold, P < 0.0001) are predicted to regulate a variety of neuronal genes that may contribute to variant host-finding behaviours. We have also found evidence for differential gene isoform usage between strains, which alters predicted microRNA interactions, and could contribute to the diversification of behaviour. Conclusions These data provide insight to the transcriptional basis of behavioural variation in S. carpocapsae, supporting efforts to understand the molecular basis of complex behaviours in nematodes.

scholarly journals Transcriptional variation and divergence of host-finding behaviour in Steinernema carpocapsae infective juveniles

2018 ◽  
Author(s):  
Neil D. Warnock ◽  
Deborah Cox ◽  
Ciaran McCoy ◽  
Robert Morris ◽  
Johnathan J. Dalzell
Keyword(s):  
Gene Expression ◽  
Target Genes ◽  
Galleria Mellonella ◽  
Entomopathogenic Nematode ◽  
Expression Patterns ◽  
Host Finding ◽  
Steinernema Carpocapsae ◽  
Differentially Expressed ◽  
Infective Juvenile ◽  
Microrna Target

AbstractSteinernema carpocapsae is an entomopathogenic nematode that employs nictation and jumping behaviours to find host insects. We aimed to investigate the transcriptional basis of variant host-finding behaviours in the infective juvenile (IJ) stage of three S. carpocapsae strains (ALL, Breton and UK1). RNA-seq analysis revealed that whilst up to 28% of the S. carpocapsae transcriptome was differentially expressed (P<0.0001) between strains, remarkably few of the most highly differentially expressed genes (>2 log2 fold change, P<0.0001) were from neuronal gene families. S. carpocapsae Breton displays increased chemotaxis toward the laboratory host Galleria mellonella, relative to the other strains. This correlates with the up-regulation of four srsx chemosensory GPCR genes, and a sodium transporter gene, asic-2, relative to both ALL and UK1 strains. The UK1 strain exhibits a decreased nictation phenotype relative to ALL and Breton strains, which correlates with co-ordinate up-regulation of neuropeptide like protein 36 (nlp-36), and down-regulation of an srt family GPCR gene, and a distinct asic-2-like sodium channel paralogue. To further investigate the link between transcriptional regulation and behavioural variation, we sequenced microRNAs across IJs of each strain. We have identified 283 high confidence microRNA genes, yielding 321 isomiR variants in S. carpocapsae, and find that up to 36% of microRNAs are differentially expressed (P<0.0001) between strains. Many of the most highly differentially expressed microRNAs (>2 log2 fold, P<0.0001) are predicted to regulate a variety of neuronal genes that may contribute to variant host-finding behaviours. We have also found evidence for differential gene isoform usage between strains, which alters predicted microRNA interactions, and could contribute to the diversification of behaviour. These data provide deeper insight to the transcriptional landscape of behavioural variation in S. carpocapsae, underpinning efforts to functionally dissect the parasite host-finding apparatus.Author summarySteinernema carpocapsae is a lethal parasite of insects. In order to find and invade a host insect, the S. carpocapsae infective juvenile will typically stand upright, waving its anterior in the air as it searches for host-specific cues. When the infective juvenile senses insect volatile compounds and movement (both signals are required), it will attempt to jump towards the source of those stimuli. Whilst the jumping behaviour is unique to Steinernema species nematodes, nictation is a host-finding behaviour shared with other important parasites of medical and veterinary importance. We have found that different strains of S. carpocpsae use modified host-finding strategies, and that these behavioural differences correlate with gene expression patterns, identifying genes that may be crucial in regulating aspects of host-finding. We also assessed the complement of microRNAs, which are small non-coding RNAs that regulate target gene expression. We found a surprising difference in the abundance of shared microRNAs between strains of S. carpocapsae; these differences also reveal expression differences that correlate with behavioural variation. Predicted microRNA target genes suggest that microRNA variation could significantly influence the behaviour of nematodes. Broadly, this study provides insight to the relationship between gene expression and behaviour, paving the way for detailed studies on gene function.

Entomopathogenic nematode host finding: response to host contact cues by cruise and ambush foragers

Parasitology ◽  
1992 ◽  
Vol 105 (2) ◽  
pp. 309-315 ◽  
Author(s):  
E.E. Lewis ◽  
R. Gaugler ◽  
R. Harrison
Keyword(s):  
Entomopathogenic Nematode ◽  
Nematode Species ◽  
Host Finding ◽  
Steinernema Carpocapsae ◽  
Foraging Strategies ◽  
Popillia Japonica ◽  
Search Behaviour ◽  
Search Area ◽  
Steinernema Glaseri ◽  
Host Cues

SUMMARYSearch behaviour of two entomopathogenic nematode species with different foraging strategies was compared by measuring parameters of unrewarded search after contact with host cues. Steinernema glaseri cruises in search of hosts. Steinernema carpocapsae ambushes hosts. Nematodes should respond to contact with relevant host cues by shifting their search from ranging to localized after contact with them. We predicted that cruising foragers rely on chemical cues more heavily than ambushers. These species were also tested for host affinities. Nematodes were tracked by image analysis after exposure to faeces, cuticle or food of either Popillia japonica or Spodoptera exiqua. Steinernema glaseri responded to selected host cues by shifting from ranging to localized search, characterized by decreased locomotory rate, distance travelled, search area and the proportion of the test period spent moving. Steinernema carpocapsae did not respond to host cues. Steinernema glaseri responds to selected chemical host cues for host location, whereas S. carpocapsae does not.

Mechanisms of specificity of association between the nematode Steinernema scapterisci and its symbiotic bacterium

Parasitology ◽  
1997 ◽  
Vol 114 (5) ◽  
pp. 483-488 ◽  
Author(s):  
P. S. GREWAL ◽  
M. MATSUURA ◽  
V. CONVERSE
Keyword(s):  
Galleria Mellonella ◽  
Entomopathogenic Nematode ◽  
Symbiotic Bacterium ◽  
Bacterial Symbiont ◽  
Steinernema Carpocapsae ◽  
Infective Juvenile ◽  
Symbiotic Bacteria ◽  
Bacterial Symbionts ◽  
First Report ◽  
Successful Isolation

We suggest a new mechanism for the maintenance of specificity of the association between the entomopathogenic nematode Steinernema scapterisci and its symbiotic bacteria. We evaluated the development and reproduction of infective and non-infective juvenile S. scapterisci in monoxenic combinations with its symbiotic bacteria, Xenorhabdus sp. ‘S’ and with the bacterial symbiont of Steinernema carpocapsae and Steinernema riobravis. Although development of non-infective stages occurred on all Xenorhabdus spp., the development of infective juveniles to the 4th stage (‘dauer’ recovery) was significantly delayed and reduced with X. nematophilus and Xenorhabdus sp. ‘R’, the bacterial symbionts of S. carpocapsae and S. riobravis, respectively. ‘Dauer’ recovery improved significantly when the cultures of X. nematophilus and Xenorhabdus sp. ‘R’ were supplemented with cell-free filtrates from Xenorhabdus sp. ‘S’. The infective juvenile S. scapterisci produced in all 3 cultures were virulent to Galleria mellonella larvae, confirming successful retention of Xenorhabdus from other steinernematids in their intestine. In fact, S. scapterisci infective juveniles containing X. nematophilus or Xenorhabdus sp. ‘R’ were more virulent to G. mellonella than those containing their natural symbiont, Xenorhabdus sp. ‘S’. We believe that this is the first demonstration of the symbiont-specific exit of infective juveniles from the ‘dauer’ phase which represents the finest level of specificity of bacteria–nematode association. This is also the first report of successful isolation of the natural symbiont of S. scapterisci.

Sex and the dynamics of infection in the entomopathogenic nematode Steinernema feltiae

1997 ◽  
Vol 71 (3) ◽  
pp. 197-202 ◽  
Author(s):  
D.A. Bohan ◽  
W.M. Hominick
Keyword(s):  
Sex Ratio ◽  
Entomopathogenic Nematodes ◽  
Galleria Mellonella ◽  
Entomopathogenic Nematode ◽  
Steinernema Feltiae ◽  
Infective Juvenile ◽  
Infective Stage ◽  
Male And Female ◽  
Per Capita ◽  
Infection Interaction

AbstractAn infection experiment was conducted to assess the change in the proportions of Steinernema feltiae Filipjev (Site 76 strain) infective juveniles becoming male or female on exposure to the test host Galleria mellonella L. Using a mathematical model for the infection interaction, the per capita probability of penetration per unit time (transmission coefficient), for those juveniles becoming male or female, and the magnitude of the male and female classes in the infective juvenile pool were estimated. The results show that S. feltiae infective juveniles which subsequently become female have a greater probability of invasion into test hosts than their male counterparts, which leads to markedly female biased sex ratios during the initial stages of the infection interaction. As the infection progresses, however, it was found that the sex ratio became balanced. This was because the underlying sex ratio in the infective stage pool was balanced. The implications of this dynamism in the sex ratio of the entomopathogenic nematodes are discussed with respect to the infection interaction, transmission and the likely environment in which the infective juveniles reside.

Entomopathogenic nematode (Heterorhabditidae and Steinernematidae) spatial distribution in turfgrass

Parasitology ◽  
1996 ◽  
Vol 113 (5) ◽  
pp. 473-482 ◽  
Author(s):  
J. F. Campbell ◽  
E. Lewis ◽  
F. Yoder ◽  
R. Gaugler
Keyword(s):  
Spatial Distribution ◽  
Vertical Distribution ◽  
Entomopathogenic Nematodes ◽  
Entomopathogenic Nematode ◽  
Soil Surface ◽  
Nematode Species ◽  
Horizontal Distribution ◽  
Steinernema Carpocapsae ◽  
Foraging Strategies ◽  
Temporal And Spatial Distribution

SUMMARYUnderstanding the temporal and spatial distribution of entomopathogenic nematodes is essential for determining the role of these insect parasites in soil communities and ultimately for their use in suppression of pest insect populations. We measured the vertical and horizontal distribution of endemic populations of entomopathogenic nematodes (Steinernema carpocapsae and Heterorhabditis bacteriophord) in turfgrass. Vertical distribution was determined by taking soil cores every 3 h from 05.00 to 23.00 h, over 4 days, and dividing the cores into 8, 1 cm deep sections. Steinernema carpocapsae was recovered primarily near the soil surface: 50% of positive sections were recovered in the thatch or first 1 cm of soil. S. carpocapsae recovery was lower during the middle of the day and none were recovered in the upper section. H. bacteriophora was recovered uniformly throughout the top 8 cm of soil and its vertical distribution did not change over the course of the day. Horizontal distribution was measured as the number of nematodes recovered from cores taken from 12 randomly selected 0·3 × 0·8 m sections from within four 15·3 × 15·3 m plots. Samples were collected biweekly over a 9-month period. H. bacteriophora had a patchier distribution than S. carpocapsae and both nematode species had more patchy distributions then their potential hosts. Our results support the hypothesis that these two species of nematode utilize different foraging strategies; S. carpocapsae primarily a surface adapted ambusher and H. bacteriophora as a cruise forager.

scholarly journals Isolation and Molecular Identification of Entomopathogenic Nematodes (Steinernema and Heterorhabditis) from East Java and Bali

2019 ◽  
Vol 14 (2) ◽  
pp. 85
Author(s):  
Chaerani Chaerani ◽  
Heri Prabowo ◽  
I G.A.A Indrayani
Keyword(s):  
Body Length ◽  
Dna Analysis ◽  
Insect Pests ◽  
Entomopathogenic Nematode ◽  
Local Environment ◽  
Nematode Species ◽  
Soil Samples ◽  
Infective Juvenile ◽  
Sequence Similarities ◽  
Diverse Habitat

<p>Entomopathogenic nematode of the families Steinernematidae and Heterorhabditidae is one of the best biological control agents of insect pests. Native isolates maybe more efficacious in controlling insect pests than imported ones because they have adapted to local environment. This study aimed to isolate and identify both nematode families from East Java and Bali<br />using DNA analysis. Sixty eight soil samples obtained from sandy soils in 16 sites of coastal regions and agricultural fields were tested for the presence of nematodes by baiting method with mealworm larvae (Tenebrio molitor). Five Heterorhabditis and two Steinernema were recovered from 7 soil samples (10% of total samples) of 7 sites (44% of total sites). Sequence analysis of<br />internal transcribed spacer (ITS) 1 and 2 regions of ribosomal DNA revealed that all Heterorhabditis belonged to indica species, with 99–100% nucleotide sequence similarities to published sequences. One of the Steinernema isolates had short infective juvenile body length (360 μm to 547 μm) and shared 99% nucleotide similarity to that of S. huense, a member of “carpocapsae” group. The other Steinernema isolate (DKS1) showed longer infective juvenile body length (from 548 μm to 762 μm) and shared 95% nucleotide similarity to the sequence of S. pakistanense, which belongs to “bicornutum” group. More detailed studies with respect to morphology are required for species confirmation of DKS1 isolate. Further exploration to<br />diverse habitat will likely to result in more previously unrecorded entomopathogenic nematode species in Indonesia.</p>

scholarly journals Spodoptera frugiperda transcriptional response to infestation by Steinernema carpocapsae

2019 ◽  
Vol 9 (1) ◽  
Author(s):  
Louise Huot ◽  
Simon George ◽  
Pierre-Alain Girard ◽  
Dany Severac ◽  
Nicolas Nègre ◽  
...  
Keyword(s):  
Spodoptera Frugiperda ◽  
Fat Body ◽  
Entomopathogenic Nematode ◽  
Transcriptional Response ◽  
Early Time ◽  
Symbiotic Bacterium ◽  
Steinernema Carpocapsae ◽  
Differentially Expressed ◽  
Xenorhabdus Nematophila ◽  
Transcriptional Responses

Abstract Steinernema carpocapsae is an entomopathogenic nematode (EPN) used in biological control of agricultural pest insects. It enters the hemocoel of its host via the intestinal tract and releases its symbiotic bacterium Xenorhabdus nematophila. In order to improve our knowledge about the physiological responses of its different hosts, we examined the transcriptional responses to EPN infestation of the fat body, the hemocytes and the midgut in the lepidopteran pest Spodoptera frugiperda. The tissues poorly respond to the infestation at an early time post-infestation of 8 h with only 5 genes differentially expressed in the fat body of the caterpillars. Strong transcriptional responses are observed at a later time point of 15 h post-infestation in all three tissues. Few genes are differentially expressed in the midgut but tissue-specific panels of induced metalloprotease inhibitors, immune receptors and antimicrobial peptides together with several uncharacterized genes are up-regulated in the fat body and the hemocytes. Among the most up-regulated genes, we identified new potential immune effectors, unique to Lepidoptera, which show homology with bacterial genes of unknown function. Altogether, these results pave the way for further functional studies of the responsive genes’ involvement in the interaction with the EPN.

Bionomics of the entomopathogenic nematode, Steinernema weiseri (Rhabditida: Steinernematidae)

Nematology ◽  
2008 ◽  
Vol 10 (5) ◽  
pp. 735-742 ◽  
Author(s):  
Ipek Bazman ◽  
Nurdan Ozer ◽  
Selcuk Hazir
Keyword(s):  
Galleria Mellonella ◽  
Entomopathogenic Nematode ◽  
Nematode Species ◽  
Head Capsule ◽  
Cold Temperatures ◽  
Larval Stages ◽  
Group 4 ◽  
Group 2 ◽  
New Generation ◽  
Steinernema Weiseri

Abstract This study describes some important bio-ecological properties of Steinernema weiseri, a recently isolated entomopathogenic nematode species in Turkey. The effects of temperature on the infectivity and development of S. weiseri were determined at 5, 8, 10, 15, 20, 25 and 30°C. The greatest and the fastest mortality of Galleria mellonella larvae was observed at 20 and 25°C (ca 2 days) and the slowest at 5°C in 11.5 days. The emergence time of the new generation of infective juveniles (IJ) from the host cadaver was shortest at 20 and 25°C (ca 9 days) and the longest at 8°C (ca 40 days). No progeny were observed at 5 and 30°C. At the tested temperatures, the lowest number of new generation IJ was obtained at 8 and 10°C and the highest at 15 and 20°C. The life cycle, determined at 23-24°C under laboratory conditions using G. mellonella as a host, took 9 days to complete. Our study suggests that the Turkish isolate of S. weiseri is adapted to cold temperatures. Steinernema weiseri has a wide host range and infects and develops well in larvae of Agrotis sp., Ceratitis capitata, Cydia splendana, Synanthedon vespiformis and Hoplocampa flava, but it infects and develops poorly in Polyphylla fullo. Larval stages of C. cossus were divided into four groups based on the diameter of their head capsules. Steinernema weiseri developed well in larval stages in Group 1 (the smallest head capsule) and Group 2 of Cossus cossus but, interestingly, very low infection and nematode development occurred in the Group 3 and Group 4 larval stage of C. cossus. No nematode infection was observed in Gryllotalpa gryllotalpa either.

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