Takema Fukatsu
Shigeyuki Kakizawa
Toshiyuki Harumoto
Akiko Sugio
Chih-Horng Kuo- 1Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology, Tsukuba, Japan
- 2Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Japan
- 3Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo, Japan
- 4Hakubi Center for Advanced Research, Kyoto University, Kyoto, Japan
- 5Graduate School of Biostudies, Kyoto University, Kyoto, Japan
- 6IGEPP, INRAE, Institut Agro, University of Rennes, Le Rheu, France
- 7Institute of Plant and Microbial Biology, Academia Sinica, Taipei, Taiwan
Editorial on the Research Topic
Spiroplasma, Mycoplasma, Phytoplasma, and other genome-reduced and wall-less mollicutes: their genetics, genomics, mechanics, interactions and symbiosis with insects, other animals and plants
Genome-reduced, wall-less, and fastidious bacteria of the genera Spiroplasma, Mycoplasma, “Candidatus Phytoplasma” and allies belonging to the class Mollicutes, are known for a number of unique microbiological features, which have prompted researchers to investigate their basic, applied, and medical aspects (Brown et al., 2018). They are mostly parasitic or symbiotic to a variety of animals or plants, living on or within the eukaryotic cells. Spiroplasmas, recognized by their characteristic helical shapes and active twitching motility, are associated with diverse arthropods and plants (Gasparich et al., 2020), and have been developed as models for the study of facultative symbionts (Anbutsu and Fukatsu, 2011; Lo et al., 2016). Some strains of Spiroplasma poulsonii and Spiroplasma ixodetis cause a remarkable reproductive phenotype, called male-killing, of their insect hosts (Hurst and Frost, 2015). In contrast, some other insect-associated spiroplasmas protect their hosts from natural enemies, including parasitoid wasps, nematodes, and pathogenic fungi (Ballinger and Perlman, 2019). Spiroplasma citri and Spiroplasma kunkelii are notorious as devastating pathogens of citrus and maize, respectively (Gasparich et al., 2020). Mycoplasmas are not only medically important as human or animal pathogens like Mycoplasma pneumoniae (Waites and Talkington, 2004) and Mycoplasma mycoides (Teodoro et al., 2020), but also intensively investigated as minimal-genome bacterial models (Yus et al., 2009). Microbial genome synthesis and engineering technologies have been developed mainly on M. mycoides and Mycoplasma capricolum (Venter et al., 2022). Some mycoplasmas are known for their capability of unique gliding motility (Miyata et al., 2020). Phytoplasmas are obligatorily parasitic to plant phloem tissues and vectored by plant-sucking insects, often causing spectacular plant morphological changes like phyllody, virescence, witches' bloom, etc. (Hogenhout et al., 2008; Bertaccini et al., 2022).
While the conventional studies have revealed fascinating aspects of this bizarre bacterial group, the whole picture of their diversity and versatility has long been elusive mainly due to their reluctance to axenic cultivation. However, owing to the recent development and availability of high-throughput DNA sequencing technologies, our knowledge on the diversity of such fastidious microbes in a variety of environments has been growing rapidly. In this context, the Research Topic “Spiroplasma, Mycoplasma, Phytoplasma, and other genome-reduced and wall-less mollicutes: their genetics, genomics, mechanics, interactions and symbiosis with insects, other animals and plants” is aimed to provide an opportunity to compile the new information emerging in this research field. In total, 10 articles and one mini review were published, of which five, three, and three articles are on Spiroplasma, Mycoplasma, Phytoplasma, respectively, thereby covering this research area in a balanced manner.
As for Spiroplasma, unique articles are contributed to this Research Topic. Mizutani, Omori et al. reported successful cloning of the whole 1.12 Mbp genome of Spiroplasma chrysopicola, which was originally isolated from a deer fly Chrysops sp., into the yeast Saccharomyces cerevisiae. Now the S. chrysopicola genome is retained in yeast cells, can be genetically engineered using sophisticated genetic tools available for S. cerevisiae, and can be distributed to anybody and utilized for further research. While a series of elaborate synthetic biological technologies have been developed using Mycoplasma spp. (Venter et al., 2022), this study serves as an initial step toward the synthetic biological approaches to Spiroplasma spp. Following two articles reported the characterization of newly obtained genomes of S. ixodetis strains. Arai et al. analyzed the genome sequence of a male-killing S. ixodetis symbiont of Homona magnanima. The genome harbored a number of putative virulence-associated genes like ankyrin domain containing genes, while no homologous sequence of spaid, a male-killing gene of S. poulsonii in Drosophila (Harumoto and Lemaitre, 2018), was identified. This implicates the diverged mechanism of male killing evolved in distinct Spiroplasma symbionts. The authors also showed bacterial tropism toward host somatic tissues and successful proliferation in various inset cell lines, which conform to the fact that S. ixodetis strains have a broad host range. Moore and Ballinger presented the complete genome sequence of a defensive S. ixodetis symbiont of D. atripex and revealed a set of toxins and virulence genes containing ribosome-inactivating protein toxin (RIP), OTU-like cysteine protease, ankyrin, and other bacterial toxin domains. They also performed a genus-wide comparative analysis of toxin/virulence-related domains between vertically transmitted and non-vertically transmitted strains, then identified a conserved core of toxin domains that is specific to the vertically transmitted strains. Kakizawa et al. highlighted the diversity of Spiroplasma as a group of facultative symbiotic bacteria of insects. The authors surveyed diverse stinkbugs representing 13 families, 69 genera, 97 species and 468 individuals, and detected Spiroplasma infection from four families (30.8%), seven genera (10.1%), 11 species (11.3%) and 21 individuals (4.5%). Phylogenetically, the stinkbug-associated Spiroplasma symbionts were placed in three distinct clades in the Spiroplasmataceae, confirming multiple and dynamic evolutionary trajectories of the stinkbug-Spiroplasma associations.
As for Mycoplasma, Mizutani, Sasajima et al. contributed a sophisticated biophysical work on the bacterial unique motility. Mycoplasma pneumoniae, known as the causative agent of mycoplasma pneumonia, binds to sialylated oligosaccharides and glides on host cell surface, which is essential for initiating the infection process (Miyata and Hamaguchi, 2016). The authors measured the stall force and the gliding speed of each M. pneumoniae cell carrying a bead that was manipulatable using optical tweezers. From the measurements of the faster strain M129 and the slower strain FH, detailed parameters of the gliding motility were measured. These results provide fundamental parameters underlying the bacterial gliding movement. Ras et al. conducted comparative genomic survey of Mycoplasma spp. for biosynthesis pathway genes of coenzyme A. The authors showed that most Mycoplasma genomes retain the genetic capacity to synthesize coenzyme A, but there was a differentiated prevalence of these genes across species. The final enzyme gene in the biosynthesis pathway encoding dephospho-coenzyme A kinase was found to be the most common among the studied Mycoplasma genomes. Yang et al. contributed a mini review about a comprehensive summary of lncRNAs and the responses of host cells associated with M. pneumoniae infections. With increasing literature on this topic, the review provided insights into the protective roles of lncRNAs against various forms of M. pneumoniae infections. They also discussed the involvement of lncRNAs in cardiovascular diseases, neurological disorders, cancers, and diabetes. Despite identifying key lncRNAs linked to M. pneumoniae pneumonia, their biological roles and mechanisms remain largely unknown. The authors emphasize the importance of understanding the molecular mechanisms of these lncRNAs.
As for Phytoplasma, two research articles provided technological advancements to facilitate the whole genome sequencing of these uncultivated pathogens from the infected plant samples. Tan et al. described an immunoprecipitation-based method for enriching the phytoplasma cells prior to DNA extraction. Zhang et al. described another enrichment method for phytoplasma cells based on serial filtration, as well as removal of host DNA using DNase I prior to the lysis of bacterial cells. By combining short read sequencing based on the Illumina platform and long read sequencing based on the Oxford Nanopore Technologies platform, both methods are effective for obtaining complete assemblies of these repeat-rich and compositionally biased genomes from metagenomic sequencing. It is worth noting that another enrichment protocol using iodixanol density gradients was developed recently and also shown to be effective (Jardim et al., 2022). In the third phytoplasma research article in this Research Topic, Huang et al. reported the first complete genome sequence of “Candidatus Phytoplasma luffae” and found that a pair of 75 kb repeats and at least 13 potential mobile units (PMUs) account for ~25% of this 769 kb chromosome. PMUs are phytoplasma-specific mobile genetic elements that often associate with effector genes (Bai et al., 2006, 2009) and likely contribute to the horizontal transfer of these virulence factors (Chung et al., 2013). In this new work, a genus-wide analysis of PMUs established a classification scheme of these mobile elements and identified strong correlations between PMU abundance and genome size at both within- and between-species levels.
In conclusion, the Research Topic presents a valuable overview of the current research coverage on Spiroplasma, Mycoplasma, and Phytoplasma, which encompasses such diverse areas as microbial diversity, genomics, reproductive manipulation, defense, toxins, biophysics and synthetic biology. These contributions highlight a variety of interesting biological phenomena observed with this wall-less, fastidious, and host-associated bacterial group. We hope that this Research Topic would provide some insight into what directions are promising in our future studies.
Author contributions
TF: Writing – original draft, Writing – review & editing. SK: Writing – review & editing. TH: Writing – review & editing. AS: Writing – review & editing. C-HK: Writing – review & editing.
Funding
The author(s) declare financial support was received for the research, authorship, and/or publication of this article. TF, SK, and TH were funded by the Japan Science and Technology Agency (JST) ERATO grant no. JPMJER1902. AS was funded by Plant2Pro-2022-R2V2 and ANR-23-CE20-0040-01 Greenpeas. C-HK was funded by Academia Sinica. AS was funded by INRAE and Agence Nationale de la Recherche (ANR).
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
The author(s) declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision.
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Keywords: Spiroplasma, Mycoplasma, Phytoplasma, symbiont, pathogen, genome, insect, plant
Citation: Fukatsu T, Kakizawa S, Harumoto T, Sugio A and Kuo C-H (2024) Editorial: Spiroplasma, Mycoplasma, Phytoplasma, and other genome-reduced and wall-less mollicutes: their genetics, genomics, mechanics, interactions and symbiosis with insects, other animals and plants. Front. Microbiol. 15:1477536. doi: 10.3389/fmicb.2024.1477536
Received: 08 August 2024; Accepted: 15 August 2024;
Published: 30 August 2024.
Edited and reviewed by: Louis S. Tisa, University of New Hampshire, United States
Copyright © 2024 Fukatsu, Kakizawa, Harumoto, Sugio and Kuo. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Takema Fukatsu, dC1mdWthdHN1JiN4MDAwNDA7YWlzdC5nby5qcA==