- Award ID(s):
- 1821533
- NSF-PAR ID:
- 10283533
- Editor(s):
- Johnson, Karyn N.
- Date Published:
- Journal Name:
- Applied and Environmental Microbiology
- Volume:
- 87
- Issue:
- 12
- ISSN:
- 0099-2240
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Johnson, Karyn N. (Ed.)ABSTRACT Leeches are found in terrestrial, aquatic, and marine habitats on all continents. Sanguivorous leeches have been used in medicine for millennia. Modern scientific uses include studies of neurons, anticoagulants, and gut microbial symbioses. Hirudo verbana , the European medicinal leech, maintains a gut community dominated by two bacterial symbionts, Aeromonas veronii and Mucinivorans hirudinis , which sometimes account for as much as 97% of the total crop microbiota. The highly simplified gut anatomy and microbiome of H. verbana make it an excellent model organism for studying gut microbial dynamics. The North American medicinal leech, Macrobdella decora , is a hirudinid leech native to Canada and the northern United States. In this study, we show that M. decora symbiont communities are very similar to those in H. verbana. We performed an extensive study using field-caught M. decora and purchased H. verbana from two suppliers. Deep sequencing of the V4 region of the 16S rRNA gene allowed us to determine that the core microbiome of M. decora consists of Bacteroides , Aeromonas, Proteocatella , and Butyricicoccus. The analysis revealed that the compositions of the gut microbiomes of the two leech species were significantly different at all taxonomic levels. The R 2 value was highest at the genus and amplicon sequence variant (ASV) levels and much lower at the phylum, class, and order levels. The gut and bladder microbial communities were distinct. We propose that M. decora is an alternative to H. verbana for studies of wild-caught animals and provide evidence for the conservation of digestive-tract and bladder symbionts in annelid models. IMPORTANCE Building evidence implicates the gut microbiome in critical animal functions such as regulating digestion, nutrition, immune regulation, and development. Simplified, phylogenetically diverse models for hypothesis testing are necessary because of the difficulty of assigning causative relationships in complex gut microbiomes. Previous research used Hirudo verbana as a tractable animal model of digestive-tract symbioses. Our data show that Macrobdella decora may work just as well without the drawback of being an endangered organism and with the added advantage of easy access to field-caught specimens. The similarity of the microbial community structures of species from two different continents reveals the highly conserved nature of the microbial symbionts in sanguivorous leeches.more » « less
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Abstract Leafhoppers comprise over 20,000 plant‐sap feeding species, many of which are important agricultural pests. Most species rely on two ancestral bacterial symbionts,
Sulcia andNasuia , for essential nutrition lacking in their phloem and xylem plant sap diets. To understand how pest leafhopper genomes evolve and are shaped by microbial symbioses, we completed a chromosomal‐level assembly of the aster leafhopper's genome (ALF;Macrosteles quadrilineatus ). We compared ALF's genome to three other pest leafhoppers,Nephotettix cincticeps ,Homalodisca vitripennis , andEmpoasca onukii , which have distinct ecologies and symbiotic relationships. Despite diverging ~155 million years ago, leafhoppers have high levels of chromosomal synteny and gene family conservation. Conserved genes include those involved in plant chemical detoxification, resistance to various insecticides, and defence against environmental stress. Positive selection acting upon these genes further points to ongoing adaptive evolution in response to agricultural environments. In relation to leafhoppers' general dependence on symbionts, species that retain the ancestral symbiont,Sulcia , displayed gene enrichment of metabolic processes in their genomes. Leafhoppers with bothSulcia and its ancient partner,Nasuia , showed genomic enrichment in genes related to microbial population regulation and immune responses. Finally, horizontally transferred genes (HTGs) associated with symbiont support ofSulcia andNasuia are only observed in leafhoppers that maintain symbionts. In contrast, HTGs involved in non‐symbiotic functions are conserved across all species. The high‐quality ALF genome provides deep insights into how host ecology and symbioses shape genome evolution and a wealth of genetic resources for pest control targets. -
Introduction Wood digestion in insects relies on the maintenance of a mosaic of numerous microhabitats, each colonized by distinct microbiomes. Understanding the division of digestive labor between these microhabitats- is central to understanding the physiology and evolution of symbiotic wood digestion. A microhabitat that has emerged to be of direct relevance to the process of lignocellulose digestion is the surface of ingested plant material. Wood particles in the guts of some termites are colonized by a specialized bacterial fiber-digesting microbiome, but whether this represents a widespread strategy among insect lineages that have independently evolved wood-feeding remains an open question.
Methods In this study, we investigated the bacterial communities specifically associated with wood fibers in the gut of the passalid beetle
Odontotaenius disjunctus . We developed a Percoll-based centrifugation method to isolate and enrich the wood particles from the anterior hindgut, allowing us to access the wood fibers and their associated microbiome. We then performed assays of enzyme activity and used short-read and long-read amplicon sequencing of the 16S rRNA gene to identify the composition of the fiber-associated microbiome.Results Our assays demonstrated that the anterior hindgut, which houses a majority of the bacterial load, is an important site for lignocellulose digestion. Wood particles enriched from the anterior hindgut contribute to a large proportion of the total enzyme activity. The sequencing revealed that
O. disjunctus , like termites, harbors a distinct fiber-associated microbiome, but notably, its community is enriched in insect-specific groups ofLactococcus andTuricibacter .Discussion Our study underscores the importance of microhabitats in fostering the complex symbiotic relationships between wood-feeding insects and their microbiomes. The discovery of distinct fiber-digesting symbionts in
O. disjunctus , compared to termites, highlights the diverse evolutionary paths insects have taken to adapt to a challenging diet.