Symbiont Recognition and Subsequent Morphogenesis as Early Events in an Animal-Bacterial Mutualism

McFall‐Ngai, Margaret J.; Ruby, Edward G.

doi:10.1126/science.1962208

Cited by 290 publications

(286 citation statements)

References 15 publications

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“…Sachs et al, 2004) or as a preferential choice of one symbiont over another irrespective of symbiont degree of cooperation (for example, Bot et al, 2001;Mueller et al, 2004). Partner choice can take place during the initiation of an association, for example, the colonization of the bobtail squid light organ by Vibrio fischeri symbionts (McFall-Ngai and Ruby, 1991;Visick et al, 2000;Nishiguchi, 2002), or as a means of avoiding cheating symbiont strains (for example, in the yucca-yucca moth symbiosis: Pellmyr and Huth, 1994;Huth and Pellmyr, 2000; in the squid-Vibrio symbiosis: Visick et al, 2000; and in the legume-Rhizobium symbiosis: Simms and Taylor, 2002;West et al, 2002). Our experiments do not evaluate if ant symbiont choice is a response to the degree of cooperation of the Pseudonocardia strains.…”

Section: Discussionmentioning

confidence: 99%

Symbiont recognition of mutualistic bacteria by Acromyrmex leaf-cutting ants

2007

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Symbiont choice has been proposed to play an important role in shaping many symbiotic relationships, including the fungus-growing ant-microbe mutualism. Over millions of years, fungusgrowing ants have defended their fungus gardens from specialized parasites with antibiotics produced by an actinomycete bacterial mutualist (genus Pseudonocardia). Despite the potential of being infected by phylogenetically diverse strains of parasites, each ant colony maintains only a single Pseudonocardia symbiont strain, which is primarily vertically transmitted between colonies by the founding queens. In this study, we show that Acromyrmex leaf-cutter ants are able to differentiate between their native actinomycete strain and a variety of foreign strains isolated from sympatric and allopatric Acromyrmex species, in addition to strains originating from other fungusgrowing ant genera. The recognition mechanism is sufficiently sensitive for the ants to discriminate between closely related symbiont strains. Our findings suggest that symbiont recognition may play a crucial role in the fungus-growing ant-bacterium mutualism, likely allowing the ants to retain ecological flexibility necessary for defending their garden from diverse parasites and, at the same time, resolve potential conflict that can arise from rearing competing symbiont strains.

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Section: Discussionmentioning

confidence: 99%

Symbiont recognition of mutualistic bacteria by Acromyrmex leaf-cutting ants

2007

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“…To camouflage themselves, squid use counterillumination from light generated by V. fischeri contained within the light organ. Juvenile squid are born without V. fischeri and must rapidly acquire and selectively populate their light organ with these symbiotic bacteria if they are to survive in the wild (McFall-Ngai and Ruby 1991). However, in the laboratory, both squid and V. fischeri can be grown independently, thereby permitting detailed study of the initiation, developmental consequences, and molecular steps necessary for this highly specific microbial symbiosis.…”

Section: Hawaiian Bobtailed Squidmentioning

confidence: 99%

Exploring host–microbiota interactions in animal models and humans

2013

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The animal and bacterial kingdoms have coevolved and coadapted in response to environmental selective pressures over hundreds of millions of years. The meta'omics revolution in both sequencing and its analytic pipelines is fostering an explosion of interest in how the gut microbiome impacts physiology and propensity to disease. Gut microbiome studies are inherently interdisciplinary, drawing on approaches and technical skill sets from the biomedical sciences, ecology, and computational biology. Central to unraveling the complex biology of environment, genetics, and microbiome interaction in human health and disease is a deeper understanding of the symbiosis between animals and bacteria. Experimental model systems, including mice, fish, insects, and the Hawaiian bobtail squid, continue to provide critical insight into how host-microbiota homeostasis is constructed and maintained. Here we consider how model systems are influencing current understanding of host-microbiota interactions and explore recent human microbiome studies.The distinctive body plans of animals offer many niches for members of the archaeal and bacterial kingdoms. While the lumen of the human distal gut is one of the most densely populated ecosystems on our planet, humans and other animals harbor several microbiomes on and within their body surfaces such as the respiratory and urogenital tracts and the skin. As the gut has evolved from the relatively simple tube of the ancient cyclostomatida to the more highly compartmentalized gastrointestinal tracts of mammalian species, the diversity and complexity of the microbial inhabitants of those spaces has increased as well (Fig.

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“…In leguminous plants, infection with symbiotic Rhizobium induces nodule formation in the root (Perret et al, 2000;Oldroyd and Downie, 2008). In Euprymna squids, infection with luminescent Vibrio fischeri is required for normal morphogenesis of the symbiotic light organ (McFall-Ngai and Ruby, 1991;Nyholm and McFall-Ngai, 2004). Whether or not the Burkholderia symbiont is involved in the formation of the host symbiotic organ is of interest, deserving future experimental and developmental studies on symbiotic and aposymbiotic insects.…”

Section: Lch90 From Leptocorisa Chinensismentioning

confidence: 99%

An ancient but promiscuous host–symbiont association between Burkholderia gut symbionts and their heteropteran hosts

2010

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Here, we investigated 124 stinkbug species representing 20 families and 5 superfamilies for their Burkholderia gut symbionts, of which 39 species representing 6 families of the superfamilies Lygaeoidea and Coreoidea were Burkholderia-positive. Diagnostic PCR surveys revealed high frequencies of Burkholderia infection in natural populations of the stinkbugs, and substantial absence of vertical transmission of Burkholderia infection to their eggs. In situ hybridization confirmed localization of the Burkholderia in their midgut crypts. In the lygaeoid and coreoid stinkbugs, development of midgut crypts in their alimentary tract was coincident with the Burkholderia infection, suggesting that the specialized morphological configuration is pivotal for establishment and maintenance of the symbiotic association. The Burkholderia symbionts were easily isolated as pure culture on standard microbiological media, indicating the ability of the gut symbionts to survive outside the host insects. Molecular phylogenetic analysis showed that the gut symbionts of the lygaeoid and coreoid stinkbugs belong to a b-proteobacterial clade together with Burkholderia isolates from soil environments and Burkholderia species that induce plant galls. On the phylogeny, the stinkbug-associated, environmental and gall-forming Burkholderia strains did not form coherent groups, indicating host-symbiont promiscuity among these stinkbugs. Symbiont culturing revealed that slightly different Burkholderia genotypes often coexist in the same insects, which is also suggestive of host-symbiont promiscuity. All these results strongly suggest an ancient but promiscuous host-symbiont relationship between the lygaeoid/coreoid stinkbugs and the Burkholderia gut symbionts. Possible mechanisms as to how the environmentally transmitted promiscuous symbiotic association has been stably maintained in the evolutionary course are discussed.

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Symbiont Recognition and Subsequent Morphogenesis as Early Events in an Animal-Bacterial Mutualism

Cited by 290 publications

References 15 publications

Symbiont recognition of mutualistic bacteria by Acromyrmex leaf-cutting ants

Symbiont recognition of mutualistic bacteria by Acromyrmex leaf-cutting ants

Exploring host–microbiota interactions in animal models and humans

An ancient but promiscuous host–symbiont association between Burkholderia gut symbionts and their heteropteran hosts

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