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1. Evolutionary history influences the microbiomes of a female symbiotic reproductive organ in cephalopods

   https://doi.org/10.1128/aem.00990-23  

   Vijayan, Nidhi ; McAnulty, Sarah J ; Sanchez, Gustavo ; Jolly, Jeffrey ; Ikeda, Yuzuru ; Nishiguchi, Michele K ; Réveillac, Elodie ; Gestal, Camino ; Spady, Blake L ; Li, Diana H ; et al ( February 2024 , Applied and Environmental Microbiology)

   Rudi, Knut (Ed.)

   Many female squids and cuttlefishes have a symbiotic reproductive organ called the accessory nidamental gland (ANG) that hosts a bacterial consortium involved with egg defense against pathogens and fouling organisms. While the ANG is found in multiple cephalopod families, little is known about the global microbial diversity of these ANG bacterial symbionts. We used 16S rRNA gene community analysis to characterize the ANG microbiome from different cephalopod species and assess the relationship between host and symbiont phylogenies. The ANG microbiome of 11 species of cephalopods from four families (superorder: Decapodiformes) that span seven geographic locations was characterized. Bacteria of classAlphaproteobacteria, Gammaproteobacteria, andFlavobacteriiawere found in all species, yet analysis of amplicon sequence variants by multiple distance metrics revealed a significant difference between ANG microbiomes of cephalopod families (weighted/unweighted UniFrac, Bray–Curtis,P= 0.001). Despite being collected from widely disparate geographic locations, members of the family Sepiolidae (bobtail squid) shared many bacterial taxa including (~50%)Opitutae(Verrucomicrobia) andRuegeria(Alphaproteobacteria) species. Furthermore, we tested for phylosymbiosis and found a positive correlation between host phylogenetic distance and bacterial community dissimilarity (Mantel testr= 0.7). These data suggest that closely related sepiolids select for distinct symbionts from similar bacterial taxa. Overall, the ANGs of different cephalopod species harbor distinct microbiomes and thus offer a diverse symbiont community to explore antimicrobial activity and other functional roles in host fitness.

   Many aquatic organisms recruit microbial symbionts from the environment that provide a variety of functions, including defense from pathogens. Some female cephalopods (squids, bobtail squids, and cuttlefish) have a reproductive organ called the accessory nidamental gland (ANG) that contains a bacterial consortium that protects eggs from pathogens. Despite the wide distribution of these cephalopods, whether they share similar microbiomes is unknown. Here, we studied the microbial diversity of the ANG in 11 species of cephalopods distributed over a broad geographic range and representing 15–120 million years of host divergence. The ANG microbiomes shared some bacterial taxa, but each cephalopod species had unique symbiotic members. Additionally, analysis of host–symbiont phylogenies suggests that the evolutionary histories of the partners have been important in shaping the ANG microbiome. This study advances our knowledge of cephalopod–bacteria relationships and provides a foundation to explore defensive symbionts in other systems.

    

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2. Persistent tissue‐specific resident microbiota in oysters across a broad geographical range

   https://doi.org/10.1111/1758-2229.70026  

   Unzueta‐Martínez, Andrea ; Bowen, Jennifer ( October 2024 , Environmental Microbiology Reports)

   Marine animals often harbour complex microbial communities that influence their physiology. However, strong evidence for resident microbiomes in marine bivalves is lacking, despite their contribution to estuarine habitats and coastal economies. We investigated whether marine bivalves harbour stable, resident microorganisms in specific tissues or if their microbiomes primarily consist of transient members reflecting the environmental microbial pool. Conducting a latitudinal study of wild eastern oysters (Crassostrea virginica) along the East Coast of the United States, we aimed to identify resident microorganisms that persist across a wide geographical range. Our results revealed that microbial communities in seawater and sediment samples followed latitudinal diversity patterns driven by geographic location. In contrast, oyster‐associated microbiomes were distinct from their surrounding environments and exhibited tissue‐specific compositions. Notably, oyster microbiomes showed greater similarity within the same tissue type across different geographic locations than among different tissue types within the same location. This indicates the presence of tissue‐specific resident microbes that persist across large geographical ranges. We identified a persistent set of resident microbiome members for each tissue type, with key microbial members consistent across all locations. These findings underscore the oyster host's role in selecting its microbiome and highlight the importance of tissue‐specific microbial communities in understanding bivalve‐associated microbiomes.

    

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3. Microbiome shifts with onset and progression of Sea Star Wasting Disease revealed through time course sampling

   https://doi.org/10.1038/s41598-018-34697-w  

   Lloyd, Melanie M. ; Pespeni, Melissa H. ( November 2018 , Scientific Reports)

   The recent outbreak of Sea Star Wasting Disease (SSWD) is one of the largest marine epizootics in history, but the host-associated microbial community changes specific to disease progression have not been characterized. Here, we sampled the microbiomes of ochre sea stars,Pisaster ochraceus, through time as animals stayed healthy or became sick and died with SSWD. We found community-wide differences in the microbiomes of sick and healthy sea stars, changes in microbial community composition through disease progression, and a decrease in species richness of the microbiome in late stages of SSWD. Known beneficial taxa (Pseudoalteromonasspp.) decreased in abundance at symptom onset and through disease progression, while known pathogenic (Tenacibaculumspp.) and putatively opportunistic bacteria (Polaribacterspp. andPhaeobacterspp.) increased in abundance in early and late disease stages. Functional profiling revealed microbes more abundant in healthy animals performed functions that inhibit growth of other microbes, including pathogen detection, biosynthesis of secondary metabolites, and degradation of xenobiotics. Changes in microbial composition with disease onset and progression suggest that a microbial imbalance of the host could lead to SSWD or be a consequence of infection by another pathogen. This work highlights the importance of the microbiome in SSWD and also suggests that a healthy microbiome may help confer resistance to SSWD.

    

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4. Microbiomes of the Sydney Rock Oyster are acquired through both vertical and horizontal transmission

   https://doi.org/10.1186/s42523-022-00186-9  

   Unzueta-Martínez, Andrea ; Scanes, Elliot ; Parker, Laura M. ; Ross, Pauline M. ; O’Connor, Wayne ; Bowen, Jennifer L. ( May 2022 , Animal Microbiome)

   The term holobiont is widely accepted to describe animal hosts and their associated microorganisms. The genomes of all that the holobiont encompasses, are termed the hologenome and it has been proposed as a unit of selection in evolution. To demonstrate that natural selection acts on the hologenome, a significant portion of the associated microbial genomes should be transferred between generations. Using the Sydney Rock Oyster (Saccostrea glomerata) as a model, we tested if the microbes of this broadcast spawning species could be passed down to the next generation by conducting single parent crosses and tracking the microbiome from parent to offspring and throughout early larval stages using 16S rRNA gene amplicon sequencing. From each cross, we sampled adult tissues (mantle, gill, stomach, gonad, eggs or sperm), larvae (D-veliger, umbo, eyed pediveliger, and spat), and the surrounding environment (water and algae feed) for microbial community analysis.

   We found that each larval stage has a distinct microbiome that is partially influenced by their parental microbiome, particularly the maternal egg microbiome. We also demonstrate the presence of core microbes that are consistent across all families, persist throughout early life stages (from eggs to spat), and are not detected in the microbiomes of the surrounding environment. In addition to the core microbiomes that span all life cycle stages, there is also evidence of environmentally acquired microbial communities, with earlier larval stages (D-veliger and umbo), more influenced by seawater microbiomes, and later larval stages (eyed pediveliger and spat) dominated by microbial members that are specific to oysters and not detected in the surrounding environment.

   Our study characterized the succession of oyster larvae microbiomes from gametes to spat and tracked selected members that persisted across multiple life stages. Overall our findings suggest that both horizontal and vertical transmission routes are possible for the complex microbial communities associated with a broadcast spawning marine invertebrate. We demonstrate that not all members of oyster-associated microbiomes are governed by the same ecological dynamics, which is critical for determining what constitutes a hologenome.

    

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5. Host–microbial systems as glass cannons: Explaining microbiome stability in corals exposed to extrinsic perturbations

   https://doi.org/10.1111/1365-2656.13466  

   Dunphy, Courtney M. ; Vollmer, Steven V. ; Gouhier, Tarik C. ( March 2021 , Journal of Animal Ecology)

   Although stability is relatively well understood in macro‐organisms, much less is known about its drivers in host–microbial systems where processes operating at multiple levels of biological organisation jointly regulate the microbiome.

   We conducted an experiment to examine the microbiome stability of three Caribbean corals (Acropora cervicornis,Pseudodiploria strigosaandPorites astreoides) by placing them in aquaria and exposing them to a pulse perturbation consisting of a large dose of broad‐spectrum antibiotics before transplanting them into the field.

   We found that coral hosts harboured persistent, species‐specific microbiomes. Stability was generally high but variable across coral species, withA. cervicornismicrobiomes displaying the lowest community turnover in both the non‐perturbed and the perturbed field transplants. Interestingly, the microbiome ofP. astreoideswas stable in the non‐perturbed field transplants, but unstable in the perturbed field transplants.

   A mathematical model of host–microbial dynamics helped resolve this paradox by showing that when microbiome regulation is driven by host sanctioning, both resistance and resilience to invasion are low and can lead to instability despite the high direct costs bourne by corals. Conversely, when microbiome regulation is mainly associated with microbial processes, both resistance and resilience to invasion are high and promote stability at no direct cost to corals. We suggest that corals that are mainly regulated by microbial processes can be likened to ‘glass cannons’ because the high stability they exhibit in the field is due to their microbiome's potent suppression of invasive microbes. However, these corals are susceptible to destabilisation when exposed to perturbations that target the vulnerable members of their microbiomes who are responsible for mounting such powerful attacks against invasive microbes. The differential patterns of stability exhibited byP. astreoidesacross perturbed and non‐perturbed field transplants suggest it is a ‘glass cannon’ whose microbiome is regulated by microbial processes, whereasA. cervicornis’ consistent patterns of stability suggest that its microbiome is mainly regulated by host‐level processes.

   Our results show that understanding how processes that operate at multiple levels of biological organisation interact to regulate microbiomes is critical for predicting the effects of environmental perturbations on host–microbial systems.

    

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