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      Detection, Detrimental Effects, and Transmission Pathways of the Pathogenic Bacterium Acaricomes phytoseiuli in Commercial Predatory Mites

      research-article
      a , b , a , c , , a , c ,
      Microbiology Spectrum
      American Society for Microbiology
      biological control, vertical transmission, cross-species infection, fluorescence localization, Neoseiulus californicus

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          ABSTRACT

          Arthropod pathogens and other microorganisms have been documented from mass production systems aimed at producing natural enemies for pest control. If losses due to pathogens are encountered in such systems, they could lead to uneconomical production of natural enemies and/or a loss of predator quality for effective field control of target pests. Here, we identify and describe the laboratory transmission of a bacterial pathogen, Acaricomes phytoseiuli, in a Chinese strain of the local predatory mite Neoseiulus californicus following contact with Phytoseiulus persimilis, a predatory mite imported for the control of small sap-sucking pests in greenhouses. Analysis of the 16S rRNA gene and whole-genome sequences of A. phytoseiuli isolated from the Chinese strain of N. californicus showed 99.6 and 99.78% similarity, respectively, to the pathogen isolated from a European population (DSM14247 strain). This is the first report of P. persimilis infected with A. phytoseiuli outside Europe and transmitting to a local predatory mite species. A. phytoseiuli severely damaged local N. californicus, leading to a dorso-ventrally flattened body and reduced prey consumption and reproduction as well as early death. Through fluorescence in situ hybridization, A. phytoseiuli was shown to accumulate in the digestive tract of mites and in the oviductal bulb of adult females. Infected males had no obvious symptoms, but they still were able to pass on the infection to healthy females through contact and mating. The pathogen was transmitted vertically to offspring by either infected parent through adherence to eggshells. A. phytoseiuli could also persist in other herbivorous arthropods from the same habitat, suggesting wider potential risks. Our study highlights pathogen risk to predators in local biocontrol industries through pathogen spread from imported material.

          IMPORTANCE Predatory mites are important natural enemies for biological control of pests, but mass rearing of the mites can be affected by pathogens. In particular, the mite pathogen Acaricomes phytoseiuli may pose a threat to predatory mite production, and we have now detected this pathogen in China. We explored the pathogen’s transmission within species, its ability to transfer to a locally important predatory mite species, and symptoms following transfer. The detection of A. phytoseiuli and its ability to transfer to a local predator where it reduces performance highlight the importance of ongoing monitoring and hygiene in the predatory mite industry.

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          Most cited references36

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          IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies

          Large phylogenomics data sets require fast tree inference methods, especially for maximum-likelihood (ML) phylogenies. Fast programs exist, but due to inherent heuristics to find optimal trees, it is not clear whether the best tree is found. Thus, there is need for additional approaches that employ different search strategies to find ML trees and that are at the same time as fast as currently available ML programs. We show that a combination of hill-climbing approaches and a stochastic perturbation method can be time-efficiently implemented. If we allow the same CPU time as RAxML and PhyML, then our software IQ-TREE found higher likelihoods between 62.2% and 87.1% of the studied alignments, thus efficiently exploring the tree-space. If we use the IQ-TREE stopping rule, RAxML and PhyML are faster in 75.7% and 47.1% of the DNA alignments and 42.2% and 100% of the protein alignments, respectively. However, the range of obtaining higher likelihoods with IQ-TREE improves to 73.3-97.1%.
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            MUSCLE: multiple sequence alignment with high accuracy and high throughput.

            We describe MUSCLE, a new computer program for creating multiple alignments of protein sequences. Elements of the algorithm include fast distance estimation using kmer counting, progressive alignment using a new profile function we call the log-expectation score, and refinement using tree-dependent restricted partitioning. The speed and accuracy of MUSCLE are compared with T-Coffee, MAFFT and CLUSTALW on four test sets of reference alignments: BAliBASE, SABmark, SMART and a new benchmark, PREFAB. MUSCLE achieves the highest, or joint highest, rank in accuracy on each of these sets. Without refinement, MUSCLE achieves average accuracy statistically indistinguishable from T-Coffee and MAFFT, and is the fastest of the tested methods for large numbers of sequences, aligning 5000 sequences of average length 350 in 7 min on a current desktop computer. The MUSCLE program, source code and PREFAB test data are freely available at http://www.drive5. com/muscle.
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              UPARSE: highly accurate OTU sequences from microbial amplicon reads.

              Amplified marker-gene sequences can be used to understand microbial community structure, but they suffer from a high level of sequencing and amplification artifacts. The UPARSE pipeline reports operational taxonomic unit (OTU) sequences with ≤1% incorrect bases in artificial microbial community tests, compared with >3% incorrect bases commonly reported by other methods. The improved accuracy results in far fewer OTUs, consistently closer to the expected number of species in a community.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                Microbiol Spectr
                Microbiol Spectr
                spectrum
                Microbiology Spectrum
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                2165-0497
                2 November 2022
                Nov-Dec 2022
                2 November 2022
                : 10
                : 6
                : e02654-22
                Affiliations
                [a ] Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
                [b ] Bio21 Institute, School of Biosciences, University of Melbournegrid.1008.9, , Parkville, Victoria, Australia
                [c ] Key Laboratory of Natural Enemies Insects, Ministry of Agriculture and Rural Affairs, Beijing, China
                South China Agricultural University
                Author notes

                The authors declare no conflict of interest.

                Author information
                https://orcid.org/0000-0001-7074-3078
                Article
                02654-22 spectrum.02654-22
                10.1128/spectrum.02654-22
                9769712
                36321911
                ae93e68d-727c-4077-b4e7-f7a9d4f405d6
                Copyright © 2022 Xie et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                History
                : 3 August 2022
                : 12 October 2022
                Page count
                supplementary-material: 0, Figures: 4, Tables: 0, Equations: 0, References: 36, Pages: 11, Words: 6527
                Funding
                Funded by: National Natural Science Foundation of China (NSFC), FundRef https://doi.org/10.13039/501100001809;
                Award ID: 32070402
                Award Recipient :
                Funded by: Natural Science Foundation of Beijing Municipality (Beijing Natural Science Foundation), FundRef https://doi.org/10.13039/501100004826;
                Award ID: 6222052
                Award Recipient :
                Funded by: CAAS | Agricultural Science and Technology Innovation Program (ASTIP), FundRef https://doi.org/10.13039/501100012421;
                Award ID: Protection and Application of Natural Enemy
                Award Recipient :
                Categories
                Research Article
                pathogenesis-and-host-response, Pathogenesis and Host Response
                Custom metadata
                November/December 2022

                biological control,vertical transmission,cross-species infection,fluorescence localization,neoseiulus californicus

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