Title: Macrobdella decora : Old World Leech Gut Microbial Community Structure Conserved in a New World Leech
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
Graf, Joerg; Nelson, Michael C.; Colston, Sophie M.
(, Microbiology Resource Announcements)
Dunning Hotopp, Julie C.
(Ed.)
ABSTRACT Aeromonas veronii strain Hm21 was isolated from the medicinal leech Hirudo verbana and is used for genetic studies. We present here the 4.71-Mbp genome with a 56-kb plasmid and identify the mutations present in strains commonly used for genetic engineering.
Berasategui, Aileen; Moller, Abraham G.; Weiss, Benjamin; Beck, Christopher W.; Bauchiero, Caroline; Read, Timothy D.; Gerardo, Nicole M.; Salem, Hassan
(, Applied and Environmental Microbiology)
Johnson, Karyn N.
(Ed.)
ABSTRACT A pervasive pest of stored leguminous products, the bean beetle Callosobruchus maculatus (Coleoptera: Chrysomelidae) associates with a simple bacterial community during adulthood. Despite its economic importance, little is known about the compositional stability, heritability, localization, and metabolic potential of the bacterial symbionts of C. maculatus . In this study, we applied community profiling using 16S rRNA gene sequencing to reveal a highly conserved bacterial assembly shared between larvae and adults. Dominated by Firmicutes and Proteobacteria , this community is localized extracellularly along the epithelial lining of the bean beetle’s digestive tract. Our analysis revealed that only one species, Staphylococcus gallinarum (phylum Firmicutes ), is shared across all developmental stages. Isolation and whole-genome sequencing of S. gallinarum from the beetle gut yielded a circular chromosome (2.8 Mb) and one plasmid (45 kb). The strain encodes complete biosynthetic pathways for the production of B vitamins and amino acids, including tyrosine, which is increasingly recognized as an important symbiont-supplemented precursor for cuticle biosynthesis in beetles. A carbohydrate-active enzyme search revealed that the genome codes for a number of digestive enzymes, reflecting the nutritional ecology of C. maculatus . The ontogenic conservation of the gut microbiota in the bean beetle, featuring a “core” community composed of S. gallinarum , may be indicative of an adaptive role for the host. In clarifying symbiont localization and metabolic potential, we further our understanding and study of a costly pest of stored products. IMPORTANCE From supplementing essential nutrients to detoxifying plant secondary metabolites and insecticides, bacterial symbionts are a key source of adaptations for herbivorous insect pests. Despite the pervasiveness and geographical range of the bean beetle Callosobruchus maculatus , the role of microbial symbioses in its natural history remains understudied. Here, we demonstrate that the bean beetle harbors a simple gut bacterial community that is stable throughout development. This community localizes along the insect’s digestive tract and is largely dominated by Staphylococcus gallinarum . In elucidating symbiont metabolic potential, we highlight its possible adaptive significance for a widespread agricultural pest.
Nobles, Sarah; Jackson, Colin R.
(, Microorganisms)
Insects that undergo metamorphosis from juveniles to adults provide an intriguing opportunity to examine the effects of life stage, species, and the environment on their gut microbiome. In this study, we surveyed the gut microbiomes of 13 species of dragonfly collected from five different locations subject to different levels of human impact. Juveniles were collected as nymphs from aquatic habitats while airborne adults were caught at the same locations. The gut microbiome was characterized by next generation sequencing of the bacterial 16S rRNA gene. Life stage was an important factor, with the gut microbiomes of dragonfly nymphs differing from those of adult dragonflies. Gut microbiomes of nymphs were influenced by sample site and, to a lesser extent, host species. Neither sample location nor host species had a strong effect on the gut microbiome of dragonfly adults. Regardless of life stage, gut microbiomes were dominated by members of the Proteobacteria, with members of the Bacteroidetes (especially in adults), Firmicutes, and Acidobacteria (especially in nymphs) also being proportionally abundant. These results demonstrate that different life stages of metamorphosing insects can harbor very different gut microbiomes and differ in how this microbiome is influenced by the surrounding environment.
Havird, Justin C.; Brannock, Pamela M.; Yoshioka, Reyn M.; Vaught, Rebecca C.; Carlson, Kaile'a; Edwards, Collin; Tracy, Allison; Twining, Cornelia W.; Zheng, Yun; Chai, David; et al
(, Limnology and Oceanography)
Abstract Animals often shape environmental microbial communities, which can in turn influence animal gut microbiomes. Invasive species in critical habitats may reduce grazing pressure from native species and shift microbial communities. The landlocked coastal ponds, pools, and caves that make up the Hawaiian anchialine ecosystem support an endemic shrimp (Halocaridina rubra) that grazes on diverse benthic microbial communities, including orange cyanobacterial‐bacterial crusts and green algal mats. Here, we asked how shrimp: (1) shape the abundance and composition of microbial communities, (2) respond to invasive fishes, and (3) whether their gut microbiomes are affected by environmental microbial communities. We demonstrate that ecologically relevant levels of shrimp grazing significantly reduce epilithon biomass. Shrimp grazed readily and grew well on both orange crusts and green mat communities. However, individuals from orange crusts were larger, despite crusts having reduced concentrations of key fatty acids. DNA profiling revealed shrimp harbor a resident gut microbiome distinct from the environment, which is relatively simple and stable across space (including habitats with different microbial communities) and time (between wild‐caught individuals and those maintained in the laboratory for >2 yr). DNA profiling also suggests shrimp grazing alters environmental microbial community composition, possibly through selective consumption and/or physical interactions. While this work suggests grazing by endemic shrimp plays a key role in shaping microbial communities in the Hawaiian anchialine ecosystem, the hypothesized drastic ecological shifts resulting from invasive fishes may be an oversimplification as shrimp may largely avoid predation. Moreover, environmental microbial communities may have little influence on shrimp gut microbiomes.
Ikuze, Edith; Cromwell, Stephanie; Ayayee, Paul; Louis, Joe
(, Diversity)
Gut microbiomes profoundly influence insect health and mediate interactions between plant hosts and their environments. Insects, including aphids, harbour diverse obligate symbionts that synthesize essential nutrients and facultative symbionts that enhance host fitness in specific ecological contexts. Sorghum (Sorghum bicolor) is a significant cereal crop cultivated worldwide that has been negatively affected by the presence of an invasive piercing-sucking insect pest, the sugarcane aphid (SCA; Melanaphis sacchari). We previously identified SC265 and SC1345 as the resistant and susceptible sorghum lines, respectively, among the founder nested association mapping (NAM) population. Here, using these resistant and susceptible lines, we explored variations in the SCA gut microbiome when they feed on two different sorghum lines with varied resistance levels. Analyses after excluding the obligate endosymbiont Buchnera aphidicola from the dataset showed a significant difference in microbial diversity and composition between resistant and susceptible sorghum lines 7- and 14 days post aphid infestation. Our results indicate that the SCA fed on susceptible and resistant sorghum lines had Pseudomonadaceae and Rhizobiaceae, respectively, as the most abundant bacterial families. Differences in gut microbial community composition were underscored by alpha diversity metrics and beta diversity compositional analyses. These findings contribute to our understanding of the intricate interplay between plant and aphid microbiomes, shedding light on potential avenues to bolster sorghum resistance to SCA.
McClure, Emily Ann, Nelson, Michael C., Lin, Amy, and Graf, Joerg. Macrobdella decora : Old World Leech Gut Microbial Community Structure Conserved in a New World Leech. Retrieved from https://par.nsf.gov/biblio/10312641. Applied and Environmental Microbiology 87.10 Web. doi:10.1128/AEM.02082-20.
McClure, Emily Ann, Nelson, Michael C., Lin, Amy, & Graf, Joerg. Macrobdella decora : Old World Leech Gut Microbial Community Structure Conserved in a New World Leech. Applied and Environmental Microbiology, 87 (10). Retrieved from https://par.nsf.gov/biblio/10312641. https://doi.org/10.1128/AEM.02082-20
McClure, Emily Ann, Nelson, Michael C., Lin, Amy, and Graf, Joerg.
"Macrobdella decora : Old World Leech Gut Microbial Community Structure Conserved in a New World Leech". Applied and Environmental Microbiology 87 (10). Country unknown/Code not available. https://doi.org/10.1128/AEM.02082-20.https://par.nsf.gov/biblio/10312641.
@article{osti_10312641,
place = {Country unknown/Code not available},
title = {Macrobdella decora : Old World Leech Gut Microbial Community Structure Conserved in a New World Leech},
url = {https://par.nsf.gov/biblio/10312641},
DOI = {10.1128/AEM.02082-20},
abstractNote = {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.},
journal = {Applied and Environmental Microbiology},
volume = {87},
number = {10},
author = {McClure, Emily Ann and Nelson, Michael C. and Lin, Amy and Graf, Joerg},
editor = {Johnson, Karyn N.}
}
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