Host and Symbiont Jointly Control Gut Microbiota during Complete Metamorphosis

Johnston, Paul R.; Rolff, Jens

doi:10.1371/journal.ppat.1005246

Cited by 154 publications

(144 citation statements)

References 49 publications

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“…Our results confirm prior culture-dependent observations (49) and a recent sequence-based study of insect adults (68) showing that a major associate of commercial G. mellonella is Enterococcus. Our results indicate for the first time that these Enterococcus spp.…”

Section: Discussionsupporting

confidence: 91%

Death Becomes Them: Bacterial Community Dynamics and Stilbene Antibiotic Production in Cadavers of Galleria mellonella Killed by Heterorhabditis and Photorhabdus spp

Wollenberg

Jagdish

Slough

et al. 2016

Appl Environ Microbiol

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Insect larvae killed by entomopathogenic nematodes are thought to contain bacterial communities dominated by a single bacterial genus, that of the nematode's bacterial symbiont. In this study, we used next-generation sequencing to profile bacterial community dynamics in greater wax moth (Galleria mellonella) larvae cadavers killed by Heterorhabditis nematodes and their Photorhabdus symbionts. We found that, although Photorhabdus strains did initially displace an Enterococcus-dominated community present in uninfected G. mellonella insect larvae, the cadaver community was not static. Twelve days postinfection, Photorhabdus shared the cadaver with Stenotrophomonas species. Consistent with this result, Stenotrophomonas strains isolated from infected cadavers were resistant to Photorhabdus-mediated toxicity in solid coculture assays. We isolated and characterized a Photorhabdus-produced antibiotic from G. mellonella cadavers, produced it synthetically, and demonstrated that both the natural and synthetic compounds decreased G. mellonella-associated Enterococcus growth, but not Stenotrophomonas growth, in vitro. Finally, we showed that the Stenotrophomonas strains described here negatively affected Photorhabdus growth in vitro. Our results add an important dimension to a broader understanding of Heterorhabditis-Photorhabdus biology and also demonstrate that interspecific bacterial competition likely characterizes even a theoretically monoxenic environment, such as a Heterorhabditis-Photorhabdus-parasitized insect cadaver. IMPORTANCEUnderstanding, and eventually manipulating, both human and environmental health depends on a complete accounting of the forces that act on and shape microbial communities. One of these underlying forces is hypothesized to be resource competition. A resource that has received little attention in the general microbiological literature, but likely has ecological and evolutionary importance, is dead/decaying multicellular organisms. Metazoan cadavers, including those of insects, are ephemeral and nutrient-rich environments, where resource competition might shape interspecific macrobiotic and microbiotic interactions. This study is the first to use a next-generation sequencing approach to study the community dynamics of bacteria within a model insect cadaver system: insect larvae parasitized by entomopathogenic nematodes and their bacterial symbionts. By integrating bioinformatic, biochemical, and classic in vitro microbiological approaches, we have provided mechanistic insight into how antibiotic-mediated bacterial interactions may shape community dynamics within insect cadavers.

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Section: Discussionsupporting

confidence: 91%

Death Becomes Them: Bacterial Community Dynamics and Stilbene Antibiotic Production in Cadavers of Galleria mellonella Killed by Heterorhabditis and Photorhabdus spp

Wollenberg

Jagdish

Slough

et al. 2016

Appl Environ Microbiol

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“…Regardless of the mechanisms, our data are consistent with Nicrophorus larvae becoming effectively sterile during pupation, an outcome previously seen in several flies and mosquitoes (45)(46)(47). It is possible that host immunity facilitates pupal symbiont suppression during metamorphosis (44,48,49), as a decline of phagocytic hemocytes and increasing phenoloxidase activity were both detected in Nicrophorus pupa (50). Following this aposymbiotic state, bacterial densities are quickly recovered at eclosion with bacterial communities that significantly overlap those present prior to pupation ( Fig.…”

Section: Discussionsupporting

confidence: 87%

Gut Microbiota Colonization and Transmission in the Burying Beetle Nicrophorus vespilloides throughout Development

Wang

Rozen

2017

Appl Environ Microbiol

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Carrion beetles in the genus Nicrophorus rear their offspring on decomposing carcasses where larvae are exposed to a diverse community of decomposer bacteria. Parents coat the carcass with antimicrobial secretions prior to egg hatch (defined as prehatch care) and also feed regurgitated food, and potentially bacteria, to larvae throughout development (defined as full care). Here, we partition the roles of prehatch and posthatch parental care in the transmission and persistence of culturable symbiotic bacteria to larvae. Using three treatment groups (full care, prehatch care only, and no care), we found that larvae receiving full care are predominantly colonized by bacteria resident in the maternal gut while larvae receiving no care are colonized with bacteria from the carcass. More importantly, larvae receiving only prehatch care were also predominantly colonized by maternal bacteria; this result indicates that parental treatment of the carcass, including application of bacteria to the carcass surface, is sufficient to ensure symbiont transfer even in the absence of direct larval feeding. Later in development, we found striking evidence that pupae undergo an aposymbiotic stage, after which they are recolonized at eclosion with bacteria similar to those found on the molted larval cuticle and on the wall of the pupal chamber. Our results clarify the importance of prehatch parental care for symbiont transmission in Nicrophorus vespilloides and suggest that these bacteria successfully outcompete decomposer bacteria during larval and pupal gut colonization.IMPORTANCE Here, we examine the origin and persistence of the culturable gut microbiota of larvae in the burying beetle Nicrophorus vespilloides. This insect is particularly interesting for this study because larvae are reared on decomposing vertebrate carcasses, where they are exposed to high densities of carrion-decomposing microbes. Larvae also receive extensive parental care in the form of carcass preservation and direct larval feeding. We find that parents transmit their gut bacteria to larvae both directly, through regurgitation, and indirectly via their effects on the carcass. In addition, we find that larvae become aposymbiotic during pupation but are recolonized apparently from bacteria shed onto the insect cuticle before adult eclosion. Our results highlight the diverse interactions between insect behavior and development on microbiota composition. They further suggest that competitive interactions mediate the bacterial composition of Nicrophorus larvae together with or apart from the influence of beetle immunity, suggesting that the bacterial communities of these insects may be highly coevolved with those of their host species.KEYWORDS Nicrophorus, parental care, symbiosis, microbiota, transmission A nimals are colonized by a diverse community of bacterial symbionts that play crucial roles in their ecology and evolution (1-3). This has been especially well studied in insects, whose bacterial symbionts can influence traits ranging from mate

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“…The observed impact of disenabling symbiosis in Lotus seemingly differs from analogous perturbations in insects and mammals, where impairment of symbiosis in the gut leads to the accumulation of pathogens and dramatic consequences for the health of the host (43)(44)(45)(46). Cologne soil-grown Lotus symbiotic mutants showed no signs of disease or altered immune response in comparison to WT ( Fig.…”

Section: Mutantsmentioning

confidence: 92%

Root nodule symbiosis in Lotus japonicus drives the establishment of distinctive rhizosphere, root, and nodule bacterial communities

Zgadzaj

Garrido‐Oter

Jensen

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

269

205

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Lotus japonicus has been used for decades as a model legume to study the establishment of binary symbiotic relationships with nitrogen-fixing rhizobia that trigger root nodule organogenesis for bacterial accommodation. Using community profiling of 16S rRNA gene amplicons, we reveal that in Lotus, distinctive noduleand root-inhabiting communities are established by parallel, rather than consecutive, selection of bacteria from the rhizosphere and root compartments. Comparative analyses of wild-type (WT) and symbiotic mutants in Nod factor receptor5 (nfr5), Nodule inception (nin) and Lotus histidine kinase1 (lhk1) genes identified a previously unsuspected role of the nodulation pathway in the establishment of different bacterial assemblages in the root and rhizosphere. We found that the loss of nitrogen-fixing symbiosis dramatically alters community structure in the latter two compartments, affecting at least 14 bacterial orders. The differential plant growth phenotypes seen between WT and the symbiotic mutants in nonsupplemented soil were retained under nitrogen-supplemented conditions that blocked the formation of functional nodules in WT, whereas the symbiosis-impaired mutants maintain an altered community structure in the nitrogen-supplemented soil. This finding provides strong evidence that the root-associated community shift in the symbiotic mutants is a direct consequence of the disabled symbiosis pathway rather than an indirect effect resulting from abolished symbiotic nitrogen fixation. Our findings imply a role of the legume host in selecting a broad taxonomic range of root-associated bacteria that, in addition to rhizobia, likely contribute to plant growth and ecological performance.Lotus japonicus | microbiota | symbiosis | 16S | nitrogen fixation

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Host and Symbiont Jointly Control Gut Microbiota during Complete Metamorphosis

Cited by 154 publications

References 49 publications

Death Becomes Them: Bacterial Community Dynamics and Stilbene Antibiotic Production in Cadavers of Galleria mellonella Killed by Heterorhabditis and Photorhabdus spp

Death Becomes Them: Bacterial Community Dynamics and Stilbene Antibiotic Production in Cadavers of Galleria mellonella Killed by Heterorhabditis and Photorhabdus spp

Gut Microbiota Colonization and Transmission in the Burying Beetle Nicrophorus vespilloides throughout Development

Root nodule symbiosis in Lotus japonicus drives the establishment of distinctive rhizosphere, root, and nodule bacterial communities

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