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1. Microbiota Perturbation or Elimination Can Inhibit Normal Development and Elicit a Starvation-Like Response in an Omnivorous Model Invertebrate

   https://doi.org/10.1128/mSystems.00802-21  

   Vera-Ponce de León, Arturo; Jahnes, Benjamin C.; Otero-Bravo, Alejandro; Sabree, Zakee L. (August 2021, mSystems)

   Klassen, Jonathan L. (Ed.)

   ABSTRACT Omnivorous animals, including humans, harbor diverse, species-rich gut communities that impact their growth, development, and homeostasis. Model invertebrates are broadly accessible experimental platforms that enable linking specific species or species groups to host phenotypes, yet often their specialized diets and distinct gut microbiota make them less comparable to human and other mammalian and gut communities. The omnivorous cockroach Periplaneta americana harbors ∼4 × 10 2 bacterial genera within its digestive tract and is enriched with taxa commonly found in omnivorous mammals (i.e., Proteobacteria, Bacteroidetes , and Firmicutes ). These features make P. americana a valuable platform for identifying microbe-mediated host phenotypes with potential translations to mammals. Rearing P. americana insects under germfree conditions resulted in prolonging development time by ∼30% and an up to ∼8% reduction in body size along three dimensions. Germfree rearing resulted in downregulation of gene networks involved in growth, energy homeostasis, and nutrient availability. Reintroduction of a defined microbiota comprised of a subset of P. americana commensals to germfree insects did not recover normal growth and developmental phenotypes or transcriptional profiles observed in conventionally reared insects. These results are in contrast with specialist-feeding model insects (e.g., Drosophila ), where introduction of a single endemic bacterial species to germfree condition-reared specimens recovered normal host phenotypes. These data suggest that understanding microbe-mediated host outcomes in animals with species-rich communities should include models that typically maintain similarly diverse microbiomes. The dramatic transcriptional, developmental, and morphological phenotypes linked to gut microbiome status in this study illustrates how microbes are key players in animal growth and evolution. IMPORTANCE Broadly accessible model organisms are essential for illustrating how microbes are engaged in the growth, development, and evolution of animals. We report that germfree rearing of omnivorous Periplaneta americana cockroaches resulted in growth defects and severely disrupted gene networks that regulate development, which highlights the importance of gut microbiota in these host processes. Absence of gut microbiota elicited a starvation-like transcriptional response in which growth and development were inhibited while nutrient scavenging was enhanced. Additionally, reintroduction of a subset of cockroach gut bacterial commensals did not broadly recover normal expression patterns, illustrating that a particular microbiome composition may be necessary for normal host development. Invertebrate microbiota model systems that enable disentangling complex, species-rich communities are essential for linking microbial taxa to specific host phenotypes. 

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2. Cultivable, Host-Specific Bacteroidetes Symbionts Exhibit Diverse Polysaccharolytic Strategies

   https://doi.org/10.1128/AEM.00091-20  

   Vera-Ponce de León, Arturo; Jahnes, Benjamin C.; Duan, Jun; Camuy-Vélez, Lennel A.; Sabree, Zakee L. (April 2020, Applied and Environmental Microbiology)

   Drake, Harold L. (Ed.)

   ABSTRACT Beneficial gut microbes can facilitate insect growth on diverse diets. The omnivorous American cockroach, Periplaneta americana (Insecta: Blattodea), thrives on a diet rich in plant polysaccharides and harbors a species-rich gut microbiota responsive to host diet. Bacteroidetes are among the most abundant taxa in P. americana and other cockroaches, based on cultivation-independent gut community profiling, and these potentially polysaccharolytic bacteria may contribute to host diet processing. Eleven Bacteroidetes isolates were cultivated from P. americana digestive tracts, and phylogenomic analyses suggest that they were new Bacteroides , Dysgonomonas , Paludibacter , and Parabacteroides species distinct from those previously isolated from other insects, humans, and environmental sources. In addition, complete genomes were generated for each isolate, and polysaccharide utilization loci (PULs) and several non-PUL-associated carbohydrate-active enzyme (CAZyme)-coding genes that putatively target starch, pectin, and/or cellulose were annotated in each of the isolate genomes. Type IX secretion system (T9SS)- and CAZyme-coding genes tagged with the corresponding T9SS recognition and export C-terminal domain were observed in some isolates, suggesting that these CAZymes were deployed via non-PUL outer membrane translocons. Additionally, single-substrate growth and enzymatic assays confirmed genomic predictions that a subset of the Bacteroides and Dysgonomonas isolates could degrade starch, pectin, and/or cellulose and grow in the presence of these substrates as a single sugar source. Plant polysaccharides enrich P. americana diets, and many of these gut isolates are well equipped to exploit host dietary inputs and potentially contribute to gut community and host nutrient accessibility. IMPORTANCE Gut microbes are increasingly being recognized as critical contributors to nutrient accessibility in animals. The globally distributed omnivorous American cockroach ( Periplaneta americana ) harbors many bacterial phyla (e.g., Bacteroidetes ) that are abundant in vertebrates. P. americana thrives on a highly diverse plant-enriched diet, making this insect a rich potential source of uncharacterized polysaccharolytic bacteria. We have cultivated, completely sequenced, and functionally characterized several novel Bacteroidetes species that are endemic to the P. americana gut, and many of these isolates can degrade simple and complex polysaccharides. Cultivation and genomic characterization of these Bacteroidetes isolates further enable deeper insight into how these taxa participate in polysaccharide metabolism and, more broadly, how they affect animal health and development. 

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3. Lack of host phylogenetic structure in the gut bacterial communities of New Zealand cicadas and their interspecific hybrids

   https://doi.org/10.1038/s41598-022-24723-3  

   Haji, Diler; Vailionis, Jason; Stukel, Mark; Gordon, Eric; Lemmon, Emily Moriarty; Lemmon, Alan R.; Simon, Chris (November 2022, Scientific Reports)

   Abstract Host-microbe interactions are intimately linked to eukaryotic evolution, particularly in sap-sucking insects that often rely on obligate microbial symbionts for nutrient provisioning. Cicadas (Cicadidae: Auchenorrhyncha) specialize on xylem fluid and derive many essential amino acids and vitamins from intracellular bacteria or fungi (Hodgkinia,Sulcia, andOphiocordyceps) that are propagated via transmission from mothers to offspring. Despite the beneficial role of these non-gut symbionts in nutrient provisioning, the role of beneficial microbiota within the gut remains unclear. Here, we investigate the relative abundance and impact of host phylogeny and ecology on gut microbial diversity in cicadas using 16S ribosomal RNA gene amplicon sequencing data from 197 wild-collected cicadas and new mitochondrial genomes across 38 New Zealand cicada species, including natural hybrids between one pair of two species. We find low abundance and a lack of phylogenetic structure and hybrid effects but a significant role of elevation in explaining variation in gut microbiota. 

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4. Early life exposure to broccoli sprouts confers stronger protection against enterocolitis development in an immunological mouse model of inflammatory bowel disease

   https://doi.org/10.1128/msystems.00688-23  

   Holcomb, Lola; Holman, Johanna M; Hurd, Molly; Lavoie, Brigitte; Colucci, Louisa; Hunt, Benjamin; Hunt, Timothy; Kinney, Marissa; Pathak, Jahnavi; Mawe, Gary M; et al (December 2023, mSystems)

   Chu, Hiutung (Ed.)

   ABSTRACT Crohn’s disease (CD) is a presentation of inflammatory bowel disease (IBD) that manifests in childhood and adolescence and involves chronic and severe enterocolitis, immune and gut microbial dysregulation, and other complications. Diet and gut-microbiota-produced metabolites are sources of anti-inflammatories that could ameliorate symptoms. However, questions remain on how IBD influences biogeographic patterns of microbial location and function in the gut, how early life transitional gut communities are affected by IBD and diet interventions, and how disruption to biogeography alters disease mediation by diet components or microbial metabolites. Many studies on diet and IBD use a chemically induced ulcerative colitis model, despite the availability of an immune-modulated CD model. Interleukin-10-knockout (IL-10-KO) mice on a C57BL/6 background, beginning at age 4 or 7 weeks, were fed a control diet or one containing 10% (wt/wt) raw broccoli sprouts, which was high in the sprout-sourced anti-inflammatory sulforaphane. Diets began 7 days prior to, and for 2 weeks after inoculation withHelicobacter hepaticus,which triggers Crohn’s-like symptoms in these immune-impaired mice. The broccoli sprout diet increased sulforaphane in plasma; decreased weight stagnation, fecal blood, and diarrhea associated; and increased microbiota richness in the gut, especially in younger mice. Sprout diets resulted in some anatomically specific bacteria in younger mice and reduced the prevalence and abundance of pathobiont bacteria which trigger inflammation in the IL-10-KO mouse, for example,Escherichia coliandHelicobacter. Overall, the IL-10-KO mouse model is responsive to a raw broccoli sprout diet and represents an opportunity for more diet-host-microbiome research. IMPORTANCETo our knowledge, IL-10-KO mice have not previously been used to investigate the interactions of host, microbiota, and broccoli, broccoli sprouts, or broccoli bioactives in resolving symptoms of CD. We showed that a diet containing 10% raw broccoli sprouts increased the plasma concentration of the anti-inflammatory compound sulforaphane and protected mice to varying degrees against disease symptoms, including weight loss or stagnation, fecal blood, and diarrhea. Younger mice responded more strongly to the diet, further reducing symptoms, as well as increased gut bacterial richness, increased bacterial community similarity to each other, and more location-specific communities than older mice on the diet intervention. Crohn’s disease disrupts the lives of patients and requires people to alter dietary and lifestyle habits to manage symptoms. The current medical treatment is expensive with significant side effects, and a dietary intervention represents an affordable, accessible, and simple strategy to reduce the burden of symptoms. 

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5. Antibiotics and fecal transfaunation differentially affect microbiota recovery, associations, and antibiotic resistance in lemur guts

   https://doi.org/10.1186/s42523-021-00126-z  

   Bornbusch, Sally L.; Harris, Rachel L.; Grebe, Nicholas M.; Roche, Kimberly; Dimac-Stohl, Kristin; Drea, Christine M. (October 2021, Animal Microbiome)

   Abstract BackgroundAntibiotics alter the diversity, structure, and dynamics of host-associated microbial consortia, including via development of antibiotic resistance; however, patterns of recovery from microbial imbalances and methods to mitigate associated negative effects remain poorly understood, particularly outside of human-clinical and model-rodent studies that focus on outcome over process. To improve conceptual understanding of host-microbe symbiosis in more naturalistic contexts, we applied an ecological framework to a non-traditional, strepsirrhine primate model via long-term, multi-faceted study of microbial community structure before, during, and following two experimental manipulations. Specifically, we administered a broad-spectrum antibiotic, either alone or with subsequent fecal transfaunation, to healthy, male ring-tailed lemurs (Lemur catta), then used 16S rRNA and shotgun metagenomic sequencing to longitudinally track the diversity, composition, associations, and resistomes of their gut microbiota both within and across baseline, treatment, and recovery phases. ResultsAntibiotic treatment resulted in a drastic decline in microbial diversity and a dramatic alteration in community composition. Whereas microbial diversity recovered rapidly regardless of experimental group, patterns of microbial community composition reflected long-term instability following treatment with antibiotics alone, a pattern that was attenuated by fecal transfaunation. Covariation analysis revealed that certain taxa dominated bacterial associations, representing potential keystone species in lemur gut microbiota. Antibiotic resistance genes, which were universally present, including in lemurs that had never been administered antibiotics, varied across individuals and treatment groups. ConclusionsLong-term, integrated study post antibiotic-induced microbial imbalance revealed differential, metric-dependent evidence of recovery, with beneficial effects of fecal transfaunation on recovering community composition, and potentially negative consequences to lemur resistomes. Beyond providing new perspectives on the dynamics that govern host-associated communities, particularly in the Anthropocene era, our holistic study in an endangered species is a first step in addressing the recent, interdisciplinary calls for greater integration of microbiome science into animal care and conservation. 

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