Bacterial cell motility of<i>Burkholderia</i> gut symbiont is required to colonize the insect gut

Lee, Jun Beom; Byeon, Jin Hee; Jang, Ho Hee; Kim, Jiyeun Kate; Yoo, Jung‐Woo; Kikuchi, Yoshitomo; Lee, Bok Luel

doi:10.1016/j.febslet.2015.08.022

Cited by 31 publications

(28 citation statements)

References 35 publications

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“…Motility is a bacterial function often required for initiating host colonization, symbiont transmission and symbiosis establishment (Ruby, 2008; Lee et al, 2015). Motility is mostly driven by flagella made of filament, basal body and motor (Ridgway, Silverman & Simon, 1977).…”

Section: Resultsmentioning

confidence: 99%

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Toward a better understanding of the mechanisms of symbiosis: a comprehensive proteome map of a nascent insect symbiont

Renoz

Champagne

Degand

et al. 2017

PeerJ

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Symbiotic bacteria are common in insects and can affect various aspects of their hosts' biology. Although the effects of insect symbionts have been clarified for various insect symbiosis models, due to the difficulty of cultivating them in vitro, there is still limited knowledge available on the molecular features that drive symbiosis. Serratia symbiotica is one of the most common symbionts found in aphids. The recent findings of freeliving strains that are considered as nascent partners of aphids provide the opportunity to examine the molecular mechanisms that a symbiont can deploy at the early stages of the symbiosis (i.e., symbiotic factors). In this work, a proteomic approach was used to establish a comprehensive proteome map of the free-living S. symbiotica strain CWBI-2.3 T . Most of the 720 proteins identified are related to housekeeping or primary metabolism. Of these, 76 were identified as candidate proteins possibly promoting host colonization. Our results provide strong evidence that S. symbiotica CWBI-2.3 T is well-armed for invading insect host tissues, and suggest that certain molecular features usually harbored by pathogenic bacteria are no longer present. This comprehensive proteome map provides a series of candidate genes for further studies to understand the molecular cross-talk between insects and symbiotic bacteria.

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Section: Resultsmentioning

confidence: 99%

“…Motility is a bacterial function that can be required for host colonization (Lee et al, 2015). Swimming motility testing was conducted according to a previously described procedure with a slight modification (Picot et al, 2004).…”

Section: Methodsmentioning

confidence: 99%

Toward a better understanding of the mechanisms of symbiosis: a comprehensive proteome map of a nascent insect symbiont

Renoz

Champagne

Degand

et al. 2017

PeerJ

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“…The N-acetylmuramoyl-L-alanine amidase enzyme in the foregut helps in cell separation during division (24). It also aids in cell motility and establishing a symbiotic association with the host (4).…”

Section: Resultsmentioning

confidence: 99%

“…Gut microbes can be either vertically or horizontally transmitted. Vertical transmission allows bacterial transfer (from the ovaries to the egg shells) to the next generation (4), whereas horizontal transmission occurs over the course of the life cycle, through diet and social behavior.…”

Section: Introductionmentioning

confidence: 99%

Survival strategies ofEnterococcus mundtiiin the gut ofSpodoptera littoralis: a live report

Mazumdar

Teh

Murali

et al. 2020

Preprint

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21The complex interaction between a higher organism and its resident gut flora is a subject of 22 immense interest in the field of symbiosis. Many insects harbor a complex community of 23 microorganisms in their gut. Larvae of Spodoptera littoralis, a lepidopteran pest which is 24 prevalent in tropical and subtropical regions of the world, have a tube-like gut structure 25 containing a simple bacterial community. This community varies both spatially (along the 26 length of the gut) and temporally (during the life cycle of the insect). 27To monitor the dynamics and rapid adaptation of microbes to the gut conditions, a GFP-tagged 28 reporter E. mundtii was constructed. After feeding to early instar S. littoralis larvae, the tagged-29 microbes recovered from the fore and hind guts by flow cytometry. The fluorescent reporter 30 confirmed the persistence of E. mundtii in the gut. RNA-sequencing of the sorted bacteria 31 highlighted various strategies that the symbiont employs to survive, including upregulated 32 pathways for tolerating alkaline stress, forming biofilms and two-component signaling systems, 33 resisting oxidative stress and quorum sensing. Although these symbionts depend on the host for 34 amino acid and fatty acids, differential regulation among various metabolic pathways points to 35 an enriched lysine synthesis pathway in the hindgut of the larvae. 36 37 animals, pests or pollinators of food crops, and as cyclers of carbon and nitrogen during the 43 decomposition of plant biomass (1) 44 There are several factors that determine the gut bacterial composition in insects. The gut can be 45 compartmentalized, resulting in structures that vary according to the complexity of the microbial 46 communities. Insects with a straight, tube-like gut usually possess a less diverse microbial 47 population compared to species with invaginations and deep pouches (1). Other factors that 48 shape the gut population include the following: oxygen level, gut pH, the presence of digestive 49 enzymes, antimicrobial compounds, and insect diet (2, 3). Although most bacteria have an 50 affinity for neutral pH, several acidophiles and alkalophiles have adapted to extreme pH 51 conditions. 52 Gut microbes can be either vertically or horizontally transmitted. Vertical transmission allows 53 bacterial transfer (from the ovaries to the egg shells) to the next generation (4), whereas 54 horizontal transmission occurs over the course of the life cycle, through diet and social behavior. 55 Regardless of how bacteria are transmitted, microbial populations may be unstable during early 56 developmental stages (5, 6). For example, in holometabolous insects, a complete metamorphosis 57 of the gut occurs in the larva, through pupal and adult stages, resulting in microbial turnover and 58 variable microbial counts (5).59 Insects are helped by their bacterial and fungal symbionts with functions relating to the digestion 60 of complex plant carbohydrates and amino acids, the assimilation of vitamins and the 61 development of defensive str...

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“…Finally, the motility of the core OS mutant strains was examined. Bacterial motility has been shown to be one of the key factors for establishing the Riptortus-Burkholderia symbiotic association (24,25). The swimming radius of bacteria strains was measured in soft agar.…”

Section: The Role Of Core Oligosaccharide Of Insect Gut Symbiontmentioning

confidence: 99%

The lipopolysaccharide core oligosaccharide of Burkholderia plays a critical role in maintaining a proper gut symbiosis with the bean bug Riptortus pedestris

Kim

Jang

Kim

et al. 2017

Journal of Biological Chemistry

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Lipopolysaccharide, the outer cell-wall component of Gram-negative bacteria, has been shown to be important for symbiotic associations. We recently reported that the lipopolysaccharide O-antigen of enhances the initial colonization of the midgut of the bean bug, However, the midgut-colonizing symbionts lack the O-antigen but display the core oligosaccharide on the cell surface. In this study, we investigated the role of the core oligosaccharide, which directly interacts with the host midgut, in the symbiosis. To this end, we generated the core oligosaccharide mutant strains, Δ, Δ, Δ and Δ and determined the chemical structures of their oligosaccharides, which exhibited different compositions. The symbiotic properties of these mutant strains were compared with those of the wild-type and O-antigen-deficient Δ strains. Upon introduction into via the oral route, the core oligosaccharide mutant strains exhibited different rates of colonization of the insect midgut. The symbiont titers in fifth-instar insects revealed significantly reduced population sizes of the inner core oligosaccharide mutant strains Δ and Δ These two strains also negatively affected host growth rate and fitness. Furthermore, individuals colonized with the Δ and Δ strains were vulnerable to septic bacterial challenge, similar to insects without a symbiont. Taken together, these results suggest that the core oligosaccharide from symbionts plays a critical role in maintaining a proper symbiont population and in supporting the beneficial effects of the symbiont on its host in the symbiosis.

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Bacterial cell motility ofBurkholderia gut symbiont is required to colonize the insect gut

Cited by 31 publications

References 35 publications

Toward a better understanding of the mechanisms of symbiosis: a comprehensive proteome map of a nascent insect symbiont

Toward a better understanding of the mechanisms of symbiosis: a comprehensive proteome map of a nascent insect symbiont

Survival strategies ofEnterococcus mundtiiin the gut ofSpodoptera littoralis: a live report

The lipopolysaccharide core oligosaccharide of Burkholderia plays a critical role in maintaining a proper gut symbiosis with the bean bug Riptortus pedestris

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