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1. Organ structure and bacterial microbiogeography in a reproductive organ of the Hawaiian bobtail squid reveal dimensions of a defensive symbiosis

   https://doi.org/10.1128/aem.02163-24  

   Kamp, Derrick L; Kerwin, Allison H; McAnulty, Sarah J; Nyholm, Spencer V (May 2025, Applied and Environmental Microbiology)

   Rudi, Knut (Ed.)

   ABSTRACT Many plants and animals house symbiotic microorganisms in specialized tissues or organs. Here, we used multidimensionalin situimaging techniques to illuminate how host organ structure and bacterial microbiogeography contribute to the symbiotic function of an organ in the Hawaiian bobtail squid,Euprymna scolopes. Along with the well-studied light organ, femaleE. scolopesharbor a community of bacteria in the accessory nidamental gland (ANG). The ANG is a dense network of epithelium-lined tubules, some of which are dominated by a single bacterial taxon. These bacteria are deposited into squid eggs, where they defend the developing embryos from harmful biofouling. This study used a combination of imaging techniques to visualize different dimensions of the ANG and its bacterial communities. Imaging entire organs with light sheet microscopy revealed that the ANG is a composite tissue of individual, non-intersecting tubules that each harbor their own bacterial population. The organ is bisected, with tubules converging toward two points at the posterior end. At these points, tubules empty into a space where bacteria can mix with squid jelly to be deposited onto eggs. Observations of the symbiotic community correlated bacterial taxa with cell morphology and revealed that tubule populations varied: some tubules contained populations of mixed taxa, whereas others contained only one bacterial genus. Together, these data shed light on how bacterial populations interact within the ANG and how the host uses physical structure to maintain and employ a symbiotic bacterial population in a defensive context.IMPORTANCESequence-based microbiome studies have revealed much about how hosts interact with communities of symbiotic microbiota but often lack a spatial understanding of how microbes relate to each other and the host in which they reside. This study uses a combination of microscopy techniques to reveal how the structure of a symbiotic organ in the female bobtail squid,Euprymna scolopes, houses diverse, beneficial bacterial populations and deploys them for egg defense. These findings suggest that spatial partitioning may be key to harboring a diverse population of antimicrobial-producing bacteria and establishing a foundation for further understanding how host structures mediate symbiotic interactions. 

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2. Fidelity varies in the symbiosis between a gutless marine worm and its microbial consortium

   https://doi.org/10.1186/s40168-022-01372-2  

   Sato, Yui; Wippler, Juliane; Wentrup, Cecilia; Ansorge, Rebecca; Sadowski, Miriam; Gruber-Vodicka, Harald; Dubilier, Nicole; Kleiner, Manuel (October 2022, Microbiome)

   Abstract BackgroundMany animals live in intimate associations with a species-rich microbiome. A key factor in maintaining these beneficial associations is fidelity, defined as the stability of associations between hosts and their microbiota over multiple host generations. Fidelity has been well studied in terrestrial hosts, particularly insects, over longer macroevolutionary time. In contrast, little is known about fidelity in marine animals with species-rich microbiomes at short microevolutionary time scales, that is at the level of a single host population. Given that natural selection acts most directly on local populations, studies of microevolutionary partner fidelity are important for revealing the ecological and evolutionary processes that drive intimate beneficial associations within animal species. ResultsIn this study on the obligate symbiosis between the gutless marine annelidOlavius algarvensisand its consortium of seven co-occurring bacterial symbionts, we show that partner fidelity varies across symbiont species from strict to absent over short microevolutionary time. Using a low-coverage sequencing approach that has not yet been applied to microbial community analyses, we analysed the metagenomes of 80O. algarvensisindividuals from the Mediterranean and compared host mitochondrial and symbiont phylogenies based on single-nucleotide polymorphisms across genomes. Fidelity was highest for the two chemoautotrophic, sulphur-oxidizing symbionts that dominated the microbial consortium of allO. algarvensisindividuals. In contrast, fidelity was only intermediate to absent in the sulphate-reducing and spirochaetal symbionts with lower abundance. These differences in fidelity are likely driven by both selective and stochastic forces acting on the consistency with which symbionts are vertically transmitted. ConclusionsWe hypothesize that variable degrees of fidelity are advantageous forO. algarvensisby allowing the faithful transmission of their nutritionally most important symbionts and flexibility in the acquisition of other symbionts that promote ecological plasticity in the acquisition of environmental resources. 

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3. White-nose syndrome restructures bat skin microbiomes

   https://doi.org/10.1128/spectrum.02715-23  

   Ange-Stark, Meghan; Parise, Katy L; Cheng, Tina L; Hoyt, Joseph R; Langwig, Kate E; Frick, Winifred F; Kilpatrick, A Marm; Gillece, John; MacManes, Matthew D; Foster, Jeffrey T (December 2023, Microbiology Spectrum)

   Ding, Xia (Ed.)

   ABSTRACT The skin microbiome is an essential line of host defense against pathogens, yet our understanding of microbial communities and how they change when hosts become infected is limited. We investigated skin microbial composition in three North American bat species (Myotis lucifugus,Eptesicus fuscus, andPerimyotis subflavus) that have been impacted by the infectious disease, white-nose syndrome, caused by an invasive fungal pathogen,Pseudogymnoascus destructans. We compared bacterial and fungal composition from 154 skin swab samples and 70 environmental samples using a targeted 16S rRNA and internal transcribed spacer amplicon approach. We found that forM. lucifugus, a species that experiences high mortality from white-nose syndrome, bacterial microbiome diversity was dramatically lower whenP. destructanswas present. Key bacterial families—including those potentially involved in pathogen defense—significantly differed in abundance in bats infected withP. destructanscompared to uninfected bats. However, skin bacterial diversity was not lower inE. fuscusorP. subflavuswhenP. destructanswas present despite populations of the latter species declining sharply from white-nose syndrome. The fungal species present on bats substantially overlapped with the fungal taxa present in the environment at the site where the bat was sampled, but fungal community composition was unaffected by the presence ofP. destructansfor any of the three bat species. This species-specific alteration in bat skin bacterial microbiomes after pathogen invasion may suggest a mechanism for the severity of white-nose syndrome inM. lucifugusbut not for other bat species impacted by the disease. IMPORTANCEInherent complexities in the composition of microbiomes can often preclude investigations of microbe-associated diseases. Instead of single organisms being associated with disease, community characteristics may be more relevant. Longitudinal microbiome studies of the same individual bats as pathogens arrive and infect a population are the ideal experiment but remain logistically challenging; therefore, investigations like our approach that are able to correlate invasive pathogens to alterations within a microbiome may be the next best alternative. The results of this study potentially suggest that microbiome-host interactions may determine the likelihood of infection. However, the contrasting relationship between Pd and the bacterial microbiomes ofMyotis lucifugusandPerimyotis subflavusindicate that we are just beginning to understand how the bat microbiome interacts with a fungal invader such as Pd. 

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4. Geography, Climate, and Habitat Shape the Microbiome of the Endangered Rock Gnome Lichen (Cetradonia linearis)

   https://doi.org/10.3390/d16030178  

   Paulsen, Julianna; Allen, Jessica L; Morris, Nathan; Dorey, Jenna; Walke, Jenifer B; Alter, S Elizabeth (March 2024, Diversity)

   Bacterial symbionts are essential components of healthy biological systems. They are increasingly recognized as important factors in the study and management of threatened species and ecosystems. Despite management shifts at the ecosystem level, microbial communities are often neglected in discussions of holobiont conservation in favor of the primary members of a symbiosis. In this study, we addressed the bacterial community knowledge gap for one of two federally endangered lichen species in the United States, Cetradonia linearis (Cladoniaceae). We collected 28 samples of the endangered rock gnome lichen (Cetradonia linearis) from 13 sites and characterized bacterial communities in thalli using 16S rRNA metabarcoding to investigate the factors influencing the microbiome composition and diversity within the thallus. We found that Proteobacteria (37.8% ± 10.3) and Acidobacteria (25.9% ± 6.0) were the most abundant phyla recovered. Cyanobacteria were a major component of the microbiome in some individuals, despite this species associating with a green algal symbiont. Habitat, climate, and geography were all found to have significant influences on bacterial community composition. An analysis of the core microbiome at a 90% threshold revealed shared amplicon sequence variants in the microbiomes of other lichens in the family Cladoniaceae. We concluded that the bacterial microbiome of Cetradonia linearis is influenced by environmental factors and that some bacterial taxa may be core to this group. Further exploration into the microbiomes of rare lichen species is needed to understand the importance of bacterial symbionts to lichen diversity and distributions. 

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5. Orientia, Rickettsia, and the microbiome in rodent attached chiggers in North Carolina, USA

   https://doi.org/10.1371/journal.pone.0311698  

   Richardson, Elise A; Garshong, Reuben; Chen, Kaiying; Crossley, Dac; Mclean, Bryan S; Wasserberg, Gideon; Apperson, Charles S; Roe, R Michael; Ponnusamy, Loganathan (December 2024, PLOS ONE)

   Ganta, Roman R (Ed.)

   Chiggers are larval mites that pose a significant health risk globally via the spread of scrub typhus. However, fundamental studies into the bacterial microbiome in North America have never been considered. In this investigation, chiggers were collected in the wild from two locally common rodent host species (i.e.,Sigmodon hispidusandPeromyscus leucopus) in three different ecoregions of North Carolina (NC), United States to investigate the composition of their bacterial communities, including potential pathogens. DNA was extracted from the chiggers, and the V3-V4 regions of the bacterial 16S rRNA gene were sequenced using next-generation sequencing (NGS). Alpha diversity metrics revealed significant differences in bacterial diversity among different collection counties. Beta diversity metrics also revealed that bacterial communities across counties were significantly different, suggesting changes in the microbiome as the environment changed. Specifically, we saw that the two western NC collection counties had similar bacterial composition as did the two eastern collection counties. In addition, we found that the chigger microbiome bacterial diversity and composition differed between rodent host species. The 16S rRNA sequence reads were assigned to 64 phyla, 106 orders, 199 families, and 359 genera. The major bacterial phylum was Actinobacteria. The most abundant species were in the generaCorynebacterium,Propionibacterium, class ZB2, andMethylobacterium. Sequences derived from potential pathogens within the generaOrientiaandRickettsiawere also detected. Our findings provide the first insights into the ecology of chigger microbiomes in the US. Further research is required to determine if the potential pathogens found detected in chiggers are a threat to humans and wildlife. 

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