Editorial: Frontiers in Wolbachia biology 2023

Wolbachia is likely the most successful endosymbiotic bacteria associated with insects and other arthropods, as well as nematodes (Werren et al., 2008). Over the past several decades, its widespread presence across the vast range of arthropod in the terrestrial ecosystem, as well as its various biological attributes, have led to an explosive development in Wolbachia research.These include the induction of striking reproductive phenotypes, namely cytoplasmic incompatibility (CI), male-killing (MK), feminization (Fem) and parthenogenesis induction (PI) (Kaur et al., 2021); obligatory and conditional beneficial fitness consequences such as nutrient provisioning and resistance to parasites, pathogens and viruses (Hamilton and Perlman, 2013;Pimental et al., 2021); essentiality for host growth, development and survival (Zug and Hammerstein, 2015;Taylor et al., 2005); and others. The biology of Wolbachia is not only a captivating area of basic research that covers host-microbe interactions ranging from cellbiology and physiology to ecology and evolution (Serbus et al., 2008;Sanaei et al., 2021), but it is also an important applied research field that contributes to Wolbachia-mediated control of vector-borne infectious diseases and pests (Iturbe-Ormaetxe et al., 2011;Ross et al., 2019), and Wolbachia-targeted prevention and remedy of filariasis (Taylor et al., 2005;Johnson et al., 2021).Since the 1 st Wolbachia Conference held at Crete, Greece, in 2000, Wolbachia Conferences have biennially provided a very active and important forum for world's researchers working on Wolbachia and other microbial symbionts of arthropods, nematodes etc. The 11 th Wolbachia Conference was initially planned to be held on 5 th -10 th July 2020, but because of the COVID pandemic, it was finally postponed to 11 th -16 th June 2023 and held so successfully. In collaboration with the 11 th Wolbachia Conference, the Research Topic "Frontiers in Wolbachia Biology 2023" was launched to provide a forum to overview achievements recently emerging in this research field. In total, twelve original research articles and two review articles are compiled in the Research Topic, which cover a variety of topics regarding the Wolbachia biology.The reproductive manipulations induced by Wolbachia infection are among the focal research topics of the Wolbachia biology. While several (putative) effector proteins responsible for CI, MK and PI phenotypes have been uncovered for several insect systems including fruit flies, mosquitoes, moths and wasps (Beckmann et al., 2017;LePage et al., 2017;Perlmutter et al., 2019;Katsuma et al., 2022;Arai et al., 2023;Fricke and Lindsay, 2024), considering the diversity of the effector molecules (Cifs, Oscar, Wmk, Pifs, etc.), more extensive survey is needed for understanding the diversity and commonality of the Wolbachia-induced Wolbachia is difficult to culture ex vivo. Thus far, several Wolbachia culture systems have been developed, where the fastidious endosymbiotic bacteria can be maintained only when cocultured with insect cell lines (Masson and Lemaitre, 2020). On the other hand, it was reported that Wolbachia purified from insect cells could be maintained in cell-free culture media for at least 1 week without loss of viability or infectivity (Rasgon et al. 2006). Here Behrmann et al.monitored the proliferation of a Wolbachia isolate from the mosquito Aedes albopictus in a host cell-free in vitro culture system by quantitative PCR. By supplementing a mosquito cell membrane fraction and fetal bovine serum, extracellular Wolbachia replication for up to 12 days was detected. Notably, even after the ex vivo maintenance for 12 days, the Wolbachia cells could establish infection to a fresh mosquito cell line, suggesting the possibility that Wolbachia might be amenable to some experimental or genetic manipulations using such cell-free culture systems. In the bedbug, the Wolbachia cells densely and endocellularly populate the well-developed symbiotic organs, called the bacteriomes, where the specific Wolbachia strain synthesizes B vitamins that are deficient in host's blood meal (Hosokawa et al., 2010;Nikoh et al., 2014). In this context, the population dynamics data of wCle in the bedbug will provide insight into how the exceptional Wolbachia strain that turned into an obligatory nutritional mutualist contributes to survival and proliferation in the life cycle of the blood-sucking insect pest that is recently reemerging worldwide (Doggett and Lee, 2023). Giordano et al. investigated reproductive performance of the soybean aphid Aphis glycines infected with or without the facultative symbionts Arsenophonus and/or Wolbachia under different aphid and soybean genotypes.These studies highlight how Wolbachia population is controlled and integrated into the endosymbiotic system in cellular, physiological and ecological contexts.Since Wolbachia is indispensable for survival and reproduction of filarial nematodes, Wolbachia-targeting drugs are regarded as promising for medical prevention and remedy of filariasis (Johnson et al., 2021). Hegde et al. reported that an azaquinazoline anti-Wolbachia agent, AWZ1066S, facilitates the sterilizing and curing effects of benzimidazole in an experimental model of filariasis. Wangwiwatsin et al. reported in silico screening of coevolving protein sequences between host filarial nematodes and their Wolbachia endosymbionts, which identified candidate "hub" genes that may connect multiple hostsymbiont interactions and thus may provide potential drug targets via disruption of host-Wolbachia interactions.For genomic and transcriptomic studies, the preparation of Wolbachia-derived DNA/RNA usually suffers heavy contamination of host-derived DNA/RNA due to the endosymbiotic nature of Wolbachia. Cantin et al. reported an improved procedure for metagenomic assembly of Wolbachia genome through selective enrichment of bacterial DNA from nematode host DNA using ATAC-seq technique. Cantin et al. also reported an improved procedure for dual RNAseq in filarial nematodes and Wolbachia endosymbionts using RNase H based ribosomal RNA depletion. These technical improvements may be useful for Wolbachia studies of not only nematodes but also insects and other arthropods.In conclusion, the Research Topic provides a valuable overview of the recent research progress in the field of Wolbachia biology. We hope that this Research Topic shows future directions of this research field, which will be manifested in the forthcoming 12 th Wolbachia Conference to be held at Okinawa, Japan, from 13 th to 19 th April 2025 (https://web.tuat.ac.jp/~insect/wolbachia2025/).

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