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Riptortus Pedestris to Prevent Secondary Bacterial Infections of Midgut Crypts

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Riptortus Pedestris to Prevent Secondary Bacterial Infections of Midgut Crypts The ISME Journal (2020) 14:1627–1638 https://doi.org/10.1038/s41396-020-0633-3 ARTICLE Burkholderia insecticola triggers midgut closure in the bean bug Riptortus pedestris to prevent secondary bacterial infections of midgut crypts 1,2,3 4,5 3 4 Yoshitomo Kikuchi ● Tsubasa Ohbayashi ● Seonghan Jang ● Peter Mergaert Received: 17 November 2019 / Revised: 3 March 2020 / Accepted: 10 March 2020 / Published online: 23 March 2020 © The Author(s), under exclusive licence to International Society for Microbial Ecology 2020 Abstract In addition to abiotic triggers, biotic factors such as microbial symbionts can alter development of multicellular organisms. Symbiont-mediated morphogenesis is well-investigated in plants and marine invertebrates but rarely in insects despite the enormous diversity of insect-microbe symbioses. The bean bug Riptortus pedestris is associated with Burkholderia insecticola which are acquired from the environmental soil and housed in midgut crypts. To sort symbionts from soil microbiota, the bean bug develops a specific organ called the “constricted region” (CR), a narrow and symbiont-selective channel, located in the midgut immediately upstream of the crypt-bearing region. In this study, inoculation of fluorescent 1234567890();,: 1234567890();,: protein-labeled symbionts followed by spatiotemporal microscopic observations revealed that after the initial passage of symbionts through the CR, it closes within 12–18 h, blocking any potential subsequent infection events. The “midgut closure” developmental response was irreversible, even after symbiont removal from the crypts by antibiotics. It never occurred in aposymbiotic insects, nor in insects infected with nonsymbiotic bacteria or B. insecticola mutants unable to cross the CR. However, species of the genus Burkholderia and its outgroup Pandoraea that can pass the CR and partially colonize the midgut crypts induce the morphological alteration, suggesting that the molecular trigger signaling the midgut closure is conserved in this bacterial lineage. We propose that this drastic and quick alteration of the midgut morphology in response to symbiont infection is a mechanism for stabilizing the insect-microbe gut symbiosis and contributes to host-symbiont specificity in a symbiosis without vertical transmission. Introduction Phenotypic alteration in response to environmental factors is Supplementary information The online version of this article (https:// omnipresent in nature, and is thought to be a driving force doi.org/10.1038/s41396-020-0633-3) contains supplementary for generation of evolutionary novelty [1]. In plants and material, which is available to authorized users. animals that are intimately associated with microbes, the * Yoshitomo Kikuchi symbiont acquisition is integrated in the hosts’ development [email protected] and sometimes triggers dramatic developmental responses. Well-known examples are found in the root nodule formation 1 Bioproduction Research Institute, National Institute of Advanced of the legume-Rhizobium symbiosis and the light organ Industrial Science and Technology (AIST), Hokkaido Center, Sapporo 062-8517, Japan morphogenesis of the squid-Vibrio symbiosis [2, 3]. Besides such drastic morphological changes in specific associations, 2 Computational Bio Big Data Open Innovation Laboratory (CBBD- OIL), AIST, Sapporo 062-8517, Japan recent studies on mammals and Drosophila gut microbiota have revealed that gut bacteria also play a significant role in 3 Graduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Japan proliferation and differentiation of gut epithelial cells and in metabolic and immunity homeostasis [4, 5]. Similarly, in the 4 Université Paris-Saclay, CEA, CNRS, Institute for Integrative Biology of the Cell (I2BC), 91198 Gif-sur-Yvette, France plant kingdom, rhizosphere microbiota modify the root and shoot architecture by modulating the phytohormone balance 5 Institute for Agro-Environmental Sciences, National Agriculture and Food Research Organization (NARO), Tsukuba 305-8604, in the plant [6]. Even nonsymbiotic, environmental bacteria Japan can have profound morphological effects on eukaryotes by 1628 Y. Kikuchi et al. the production of small molecules that act as essential perfectly tight and some allied nonsymbiont Burkholderia developmental cues. The settlement and subsequent meta- species as well as species of its outgroup Pandoraea can morphosis of free-swimming larvae of the marine tubeworm nevertheless penetrate the CR [36]. Interestingly, the non- Hydroides elegans are trigged by biofilms of the bacterium native Burkholderia and Pandoraea species do not fully Pseudoalteromonas luteoviolacea. These biofilms deliver a occupy the lumen of the midgut crypts and co-inoculation metamorphosis-triggering effector protein into the larvae analyses revealed that B. insecticola always outcompetes via a contractile injection system [7–9]. Another striking these non-native bacteria inside the crypts, suggesting that example is the triggering of multicellularity from a single the crypt’s luminal environment favors only the native founder cell in the choanoflagellate Salpingoaeca rosetta symbiont [36]. Although the molecular basis remains by a sulfonolipid, derived from specificpreybacteriaofthe unclear, the competition-based winnowing is therefore, Bacteroidetes [10]. thought of as a second-line mechanism ensuring the host- The class Insecta consists of over one million described symbiont specificity. In addition to these partner choice species and is the most diverse animal group in the terres- mechanisms, here we discovered a third mechanism trial ecosystem. Many insects harbor symbiotic bacteria in underpinning the specific gut symbiosis which we call specialized cells called bacteriocytes or in gut crypts “midgut closure”, wherein the CR is closed immediately [11, 12]. In these symbiotic organs, bacterial symbionts play after colonization of the crypt-bearing midgut region by the metabolic roles for the hosts, such as provision of essential symbiont, preventing subsequent infections. nutrients and/or digestion of indigestible food materials [13–15]. Recent studies have revealed that, in addition, symbionts alter diverse aspects of host phenotypes, Materials and methods including heat tolerance, pathogen resistance, behavior, sex, cuticle hardening, body color, and tolerance to phytotoxins Insects and bacterial strains and insecticides [16–23]. Despite the accumulated knowl- edge about the diverse symbiosis-mediated phenotypes, The strain of R. pedestris used in this study was originally symbiont-induced morphogenesis of the symbiotic organ collected from a soybean (Glycine max) field in Tsukuba, has been poorly described in insects. Ibaraki, Japan, and maintained in the laboratory over ten The bean bug Riptortus pedestris develops a number of years. The insects were reared in petri dishes (90 mm in crypts in a posterior region of the midgut, the lumen of diameter and 20 mm high) at 25 °C under a long-day regi- which is densely colonized by the betaproteobacterial men (16 h light, 8 h dark) and fed with soybean seeds and symbiont, Burkholderia insecticola [24–27]. Infection with distilled water containing 0.05% ascorbic acid (DWA). For B. insecticola improves growth and fecundity of the bean inoculation tests of fluorescent-protein-labeled B. insecti- bug [28] probably because the symbiont recycles host cola, a green fluorescent protein (GFP)-labeled strain, metabolic wastes in the midgut crypts [29]. Unlike the RPE225 [28], and a red fluorescent protein (RFP)-labeled typical insect-microbe symbioses in which symbionts are strain, KT39 [36], were used. B. insecticola derivatives, vertically transmitted from mother to offspring, the bean including gene-deletion mutants, and nonsymbiotic bacteria bug acquires B. insecticola from environmental soil every used in this study are listed in Supplementary Table S1. generation [30]. From hatching to adulthood, the bean bug They were labeled with GFP using the Tn7 minitransposon development passes over five instar stages and the symbiont system, as previously described [28, 37]. is acquired preferentially at the 2nd instar but also 3rd instar nymphs are compatible for infection [31]. Oral inoculation of cultured symbiont cells Since diverse microorganisms abound in the environ- ment, particularly in soils [32], hosts need to sort their The symbiont strains were grown to early log phase in YG specific partner from this microbial community. Further- medium (containing 30 µg/ml kanamycin for GFP-labeled more, after symbiont colonization, they have to protect the RPE225 and RFP-labeled KT39) on a gyratory shaker symbiotic organ against invasion by superinfection to sta- (150 rpm) at 30 °C. Bacteria were harvested by centrifuga- bilize the mutualistic association. To sort the symbiont, the tion, resuspended in DWA, and adjusted to 104 cells/µl bean bug develops a specific organ called the “constricted in DWA. Three types of inoculations were performed: region” (CR), a narrow passage filled with a mucus-like (i) oral inoculation of the GFP strain at the 2nd instar, matrix, located in the midgut immediately upstream of the (ii) oral inoculation of the GFP strain at the 3rd instar, and crypt-bearing region [33]. The CR sorts out contaminating (iii) oral inoculation of the RFP strain at the 2nd and then microorganisms while B. insecticola can penetrate into the the GFP strain inoculated after a defined interval. symbiotic region using an unusual, corkscrew-like flagellar (i) Oral inoculation
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