Can microorganisms assist the survival and parasitism of plant-parasitic nematodes?

Topalović, Olivera; Vestergård, Mette

doi:10.1016/j.pt.2021.05.007

Cited by 25 publications

(19 citation statements)

References 75 publications

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“…Host-associated microbes may play significant roles in the rhizosphere, but the complexity of these environments can make them challenging to study. Diverse microbiota has been detected in nematodes, whose communities number in the millions per m 2 in the rhizosphere ( Bongers and Ferris, 1999 ; Adam et al, 2014 ; Ferris and Tuomisto, 2015 ; Elhady et al, 2017 ; Zheng et al, 2020 ; Topalović and Vestergård, 2021 ). Such microbes may facilitate plant-feeding in rhizosphere organisms, as has been observed in above-ground plant-feeders, in which symbionts supplement essential nutrients ( Moran et al, 2008 ; Bennett and Moran, 2013 ) or synthesize protective toxins or plant toxin-degrading enzymes ( Cheng et al, 2013 ; Douglas, 2015 ; Gressel, 2018 ).…”

Section: Introductionmentioning

confidence: 99%

Discovery of Early-Branching Wolbachia Reveals Functional Enrichment on Horizontally Transferred Genes

2022

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Wolbachia is a widespread endosymbiont of insects and filarial nematodes that profoundly influences host biology. Wolbachia has also been reported in rhizosphere hosts, where its diversity and function remain poorly characterized. The discovery that plant-parasitic nematodes (PPNs) host Wolbachia strains with unknown roles is of interest evolutionarily, ecologically, and for agriculture as a potential target for developing new biological controls. The goal of this study was to screen communities for PPN endosymbionts and analyze genes and genomic patterns that might indicate their role. Genome assemblies revealed 1 out of 16 sampled sites had nematode communities hosting a Wolbachia strain, designated wTex, that has highly diverged as one of the early supergroup L strains. Genome features, gene repertoires, and absence of known genes for cytoplasmic incompatibility, riboflavin, biotin, and other biosynthetic functions placed wTex between mutualist C + D strains and reproductive parasite A + B strains. Functional terms enriched in group L included protoporphyrinogen IX, thiamine, lysine, fatty acid, and cellular amino acid biosynthesis, while dN/dS analysis suggested the strongest purifying selection on arginine and lysine metabolism, and vitamin B6, heme, and zinc ion binding, suggesting these as candidate roles in PPN Wolbachia. Higher dN/dS pathways between group L, wPni from aphids, wFol from springtails, and wCfeT from cat fleas suggested distinct functional changes characterizing these early Wolbachia host transitions. PPN Wolbachia had several putative horizontally transferred genes, including a lysine biosynthesis operon like that of the mitochondrial symbiont Midichloria, a spirochete-like thiamine synthesis operon shared only with wCfeT, an ATP/ADP carrier important in Rickettsia, and a eukaryote-like gene that may mediate plant systemic acquired resistance through the lysine-to-pipecolic acid system. The Discovery of group L-like variants from global rhizosphere databases suggests diverse PPN Wolbachia strains remain to be discovered. These findings support the hypothesis of plant-specialization as key to shaping early Wolbachia evolution and present new functional hypotheses, demonstrating promise for future genomics-based rhizosphere screens.

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Section: Introductionmentioning

confidence: 99%

Discovery of Early-Branching Wolbachia Reveals Functional Enrichment on Horizontally Transferred Genes

2022

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“…Insects facing EPN associated with mutualistic bacteria co-evolved with them for millions of years, allowing the development of complex resistance mechanisms [ 5 ]. Several studies have reported that the composition of insect host microbiota is closely linked to the course of nematode parasitism [ 45 , 46 ]. Whether these resistance mechanisms, in addition to the activation of the immune response, avoidance behaviors, or morphological barriers, might include a selection of specific protective-acting microbes is still an open question.…”

Section: Discussionmentioning

confidence: 99%

“…For example, certain bacterial endosymbionts of insects, Wolbachia and Spiroplasma spp., were found to be able to impede the growth of Brugia and Howardula spp. nematodes, which infect mosquitos and fruit flies, respectively [ 45 , 46 ]. Insect endosymbionts with antimicrobial activity, which are widespread in beetles, can also play an important role in the regulation of insect host–nematode interaction [ 47 , 48 ].…”

Section: Discussionmentioning

confidence: 99%

“…It has been determined that EPN IJs highly transcribe genes coding for venom proteins already in the host-seeking stage, to be ready for their activation in the insect host; however, there are no data on the effects of these products on the host microbiota [ 55 ]. It is also known that other parasitic nematodes exhibit broad antimicrobial activity by secreting antibacterial factors such as lysozymes, cecropins, or C-type lectins; therefore, they can limit the growth of certain microbes and enrich the gut environment with nematode-protective microbiota members, supporting the suppression of host immunity and facilitating infection [ 45 , 56 , 57 , 58 ]. In addition, EPN mutualists are able to colonize the midgut, substantially affecting its microbiota, since they not only utilize gut nutrients but are also able to secrete a broad spectrum of antibiotics [ 59 , 60 ].…”

Section: Discussionmentioning

confidence: 99%

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Comparative Nanopore Sequencing-Based Evaluation of the Midgut Microbiota of the Summer Chafer (Amphimallon solstitiale L.) Associated with Possible Resistance to Entomopathogenic Nematodes

Sajnaga

Skowronek

Kalwasińska

et al. 2022

IJERPH

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Root-feeding Amphimallon solstitiale larvae and certain other scarab beetles are the main soil-dwelling pests found in Europe, while entomopathogenic nematodes (EPN) have been used as a biocontrol agent against these species. Our study provides the first detailed characterization of the bacterial community of the midgut in wild A. solstitiale larvae, based on the nanopore sequencing of the 16S rRNA gene. In the whole dataset, we detected 2586 different genera and 11,641 species, with only 83 diverse bacterial genera shared by all studied individuals, which may represent members of the core midgut microbiota of A. solstitiale larvae. Subsequently, we compared the midgut microbiota of EPN-resistant and T0 (prior to EPN exposure) individuals, hypothesizing that resistance to this parasitic infection may be linked to the altered gut community. Compared to the control, the resistant insect microbiota demonstrated lower Shannon and Evenness indices and significant differences in the community structure. Our studies confirmed that the gut microbiota alternation is associated with resistant insects; however, there are many processes involved that can affect the bacterial community. Further research on the role of gut microbiota in insect-parasitic nematode interaction may ultimately lead to the improvement of biological control strategies in insect pest management.

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“…Followup studies may as well explore the possible mechanisms of R. similis suppression in the non-sterile rhizosphere, which may include direct parasitism or predation on the nematode or its eggs (Sikora et al, 2008;Li et al, 2015), antibiosis through production of toxic metabolites (Mwaura et al, 2010;Keswani et al, 2020), competition for nutrients and other resources (Kerry, 2000), as well as induced systemic resistance (Sikora et al, 2008;Walters, 2009;Paparu et al, 2013;Poveda et al, 2020). Such studies may be complemented with those assessing microorganisms that assist the survival and parasitism of plantparasitic nematodes by protecting them against antagonistic microbes (Topalović and Vestergård, 2021). It should also be considered that microbes such as arbuscular mycorrhizal (AM) fungi known to be beneficial to host plants may also suppress plant growth while increasing infections by plantparasitic nematodes (Frew et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

Soil Microbes Determine Outcomes of Pathogenic Interactions Between Radopholus similis and Fusarium oxysporum V5w2 in Tissue Culture Banana Rhizospheres Starved of Nitrogen, Phosphorus, and Potassium

Ochieno

2022

Front. Sustain. Food Syst.

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The contributions of soil biota toward outcomes of pathogenic interactions between Radopholus similis and Fusarium oxysporum V5w2 in tissue culture banana plants starved of nitrogen (N), phosphorus (P), and potassium (K) were investigated. The study was based on three screenhouse factorial experiments (2 × 2 × 2) comprising of potted banana plants with or without R. similis, with or without F. oxysporum V5w2, and either grown in sterile or non-sterile soil. All plants in each of the three experiments received nutrient solutions that were deficient in N, P, or K, respectively. In all the three nutritional regimes, plants inoculated with R. similis were heavily colonized by the nematode with high percentage dead roots and necrosis, while their root biomasses were low. N-starved plants co-inoculated with R. similis and F. oxysporum V5w2 had lower percentage dead roots and tended to have numerically lower nematode density compared to those treated with R. similis only, especially in non-sterile soil. N-starved plants inoculated with R. similis had higher shoot dry weight, were taller with more leaves that were larger, compared to those not inoculated with the nematode. Plants grown in non-sterile soil had lower percentage dead roots, necrosis and R. similis density than those from sterile soil, regardless of the nutrient regime. N-starved plants from non-sterile soil were shorter with smaller leaves having decreased chlorophyll content and lower biomass, compared to those from sterile soil. By contrast, P and K starved plants from non-sterile soil were taller with larger leaves and more biomass, compared to those from sterile soil. Roots inoculated with R. similis had higher endophytic colonization by Fusarium spp., especially when co-inoculated with F. oxysporum V5w2 and grown in sterile soil among the N and K-starved plants. In conclusion, pathogenic interactions between R. similis and F. oxysporum V5w2 are predominantly suppressed by a complex of soil microbes that exert plant growth promoting effects in tissue culture banana plants through N, P, and K dependent processes. Nitrogen is the most important limiting factor in rhizosphere interactions between banana roots, beneficial microbes and the pathogens. Soil sterilization and the stringent aseptic tissue culture techniques still require the development of alternative innovative ways of conserving microbial services for sustainable agriculture.

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Can microorganisms assist the survival and parasitism of plant-parasitic nematodes?

Cited by 25 publications

References 75 publications

Discovery of Early-Branching Wolbachia Reveals Functional Enrichment on Horizontally Transferred Genes

Discovery of Early-Branching Wolbachia Reveals Functional Enrichment on Horizontally Transferred Genes

Comparative Nanopore Sequencing-Based Evaluation of the Midgut Microbiota of the Summer Chafer (Amphimallon solstitiale L.) Associated with Possible Resistance to Entomopathogenic Nematodes

Soil Microbes Determine Outcomes of Pathogenic Interactions Between Radopholus similis and Fusarium oxysporum V5w2 in Tissue Culture Banana Rhizospheres Starved of Nitrogen, Phosphorus, and Potassium

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