More Like this

1. Maturation state of colonization sites promotes symbiotic resiliency in the Euprymna scolopes-Vibrio fischeri partnership

   https://doi.org/10.1186/s40168-023-01509-x  

   Essock-Burns, Tara ; Lawhorn, Susannah ; Wu, Leo ; McClosky, Sawyer ; Moriano-Gutierrez, Silvia ; Ruby, Edward G. ; McFall-Ngai, Margaret J. ( March 2023 , Microbiome)

   Many animals and plants acquire their coevolved symbiotic partners shortly post-embryonic development. Thus, during embryogenesis, cellular features must be developed that will promote both symbiont colonization of the appropriate tissues, as well as persistence at those sites. While variation in the degree of maturation occurs in newborn tissues, little is unknown about how this variation influences the establishment and persistence of host-microbe associations.

   The binary symbiosis model, the squid-vibrio (Euprymna scolopes-Vibrio fischeri) system, offers a way to study how an environmental gram-negative bacterium establishes a beneficial, persistent, extracellular colonization of an animal host. Here, we show that bacterial symbionts occupy six different colonization sites in the light-emitting organ of the host that have both distinct morphologies and responses to antibiotic treatment.Vibrio fischeriwas most resilient to antibiotic disturbance when contained within the smallest and least mature colonization sites. We show that this variability in crypt development at the time of hatching allows the immature sites to act as a symbiont reservoir that has the potential to reseed the more mature sites in the host organ when they have been cleared by antibiotic treatment. This strategy may produce an ecologically significant resiliency to the association.

   The data presented here provide evidence that the evolution of the squid-vibrio association has been selected for a nascent organ with a range of host tissue maturity at the onset of symbiosis. The resulting variation in physical and chemical environments results in a spectrum of host-symbiont interactions, notably, variation in susceptibility to environmental disturbance. This “insurance policy” provides resiliency to the symbiosis during the critical period of its early development. While differences in tissue maturity at birth have been documented in other animals, such as along the infant gut tract of mammals, the impact of this variation on host-microbiome interactions has not been studied. Because a wide variety of symbiosis characters are highly conserved over animal evolution, studies of the squid-vibrio association have the promise of providing insights into basic strategies that ensure successful bacterial passage between hosts in horizontally transmitted symbioses.

    

   more » « less
2. Interactions of Symbiotic Partners Drive the Development of a Complex Biogeography in the Squid-Vibrio Symbiosis

   https://doi.org/10.1128/mBio.00853-20  

   Essock-Burns, Tara ; Bongrand, Clotilde ; Goldman, William E. ; Ruby, Edward G. ; McFall-Ngai, Margaret J. ; Graf, Joerg ( June 2020 , mBio)

   ABSTRACT Microbes live in complex microniches within host tissues, but how symbiotic partners communicate to create such niches during development remains largely unexplored. Using confocal microscopy and symbiont genetics, we characterized the shaping of host microenvironments during light organ colonization of the squid Euprymna scolopes by the bacterium Vibrio fischeri . During embryogenesis, three pairs of invaginations form sequentially on the organ’s surface, producing pores that lead to interior compressed tubules at different stages of development. After hatching, these areas expand, allowing V. fischeri cells to enter and migrate ∼120 μm through three anatomically distinct regions before reaching blind-ended crypt spaces. A dynamic gatekeeper, or bottleneck, connects these crypts with the migration path. Once V. fischeri cells have entered the crypts, the bottlenecks narrow, and colonization by the symbiont population becomes spatially restricted. The actual timing of constriction and restriction varies with crypt maturity and with different V. fischeri strains. Subsequently, starting with the first dawn following colonization, the bottleneck controls a lifelong cycle of dawn-triggered expulsions of most of the symbionts into the environment and a subsequent regrowth in the crypts. Unlike other developmental phenotypes, bottleneck constriction is not induced by known microbe-associated molecular patterns (MAMPs) or by V. fischeri - produced bioluminescence, but it does require metabolically active symbionts. Further, while symbionts in the most mature crypts have a higher proportion of live cells and a greater likelihood of expulsion at dawn, they have a lower resistance to antibiotics. The overall dynamics of these distinct microenvironments reflect the complexity of the host-symbiont dialogue. IMPORTANCE The complexity, inaccessibility, and time scales of initial colonization of most animal microbiomes present challenges for the characterization of how the bacterial symbionts influence the form and function of tissues in the minutes to hours following the initial interaction of the partners. Here, we use the naturally occurring binary squid-vibrio association to explore this phenomenon. Imaging of the spatiotemporal landscape of this symbiosis during its onset provides a window into the impact of differences in both host-tissue maturation and symbiont strain phenotypes on the establishment of a dynamically stable symbiotic system. These data provide evidence that the symbionts shape the host-tissue landscape and that tissue maturation impacts the influence of strain-level differences on the daily rhythms of the symbiosis, the competitiveness for colonization, and antibiotic sensitivity. 

   more » « less
3. Persistent symbiont colonization leads to a maturation of hemocyte response in the Euprymna scolopes / Vibrio fischeri symbiosis

   https://doi.org/10.1002/mbo3.858  

   Rader, Bethany ; McAnulty, Sarah J. ; Nyholm, Spencer V. ( June 2019 , MicrobiologyOpen)

   The binary association between the squid,Euprymna scolopes, and its symbiont,Vibrio fischeri, serves as a model system to study interactions between beneficial bacteria and the innate immune system. Previous research demonstrated that binding of the squid's immune cells, hemocytes, toV. fischeriis altered if the symbiont is removed from the light organ, suggesting that host colonization alters hemocyte recognition ofV. fischeri. To investigate the influence of symbiosis on immune maturation during development, we characterized hemocyte binding and phagocytosis ofV. fischeriand nonsymbioticVibrio harveyifrom symbiotic (sym) and aposymbiotic (apo) juveniles, and wild‐caught and laboratory‐raised sym and apo adults. Our results demonstrate that while light organ colonization byV. fischeridid not alter juvenile hemocyte response, these cells bound a similar number ofV. fischeriandV. harveyiyet phagocytosed onlyV. harveyi. Our results also indicate that long‐term colonization altered the adult hemocyte response toV. fischeribut notV. harveyi. All hemocytes from adult squid, regardless of apo or sym state, both bound and phagocytosed a similar number ofV. harveyiwhile hemocytes from both wild‐caught and sym‐raised adults bound significantly fewerV. fischeri, although moreV. fischeriwere phagocytosed by hemocytes from wild‐caught animals. In contrast, hemocytes from apo‐raised squid bound similar numbers of bothV. fischeriandV. harveyi, although moreV. harveyicells were engulfed, suggesting that blood cells from apo‐raised adults behaved similarly to juvenile hosts. Taken together, these data suggest that persistent colonization by the light organ symbiont is required for hemocytes to differentially bind and phagocytoseV. fischeri. The cellular immune system ofE. scolopeslikely possesses multiple mechanisms at different developmental stages to promote a specific and life‐long interaction with the symbiont.

    

   more » « less
4. Genomic analysis reveals an exogenous viral symbiont with dual functionality in parasitoid wasps and their hosts

   https://doi.org/10.1371/journal.ppat.1009069  

   Coffman, Kelsey A. ; Burke, Gaelen R. ( November 2020 , PLOS Pathogens)

   Roossinck, Marilyn J. (Ed.)

   Insects are known to host a wide variety of beneficial microbes that are fundamental to many aspects of their biology and have substantially shaped their evolution. Notably, parasitoid wasps have repeatedly evolved beneficial associations with viruses that enable developing wasps to survive as parasites that feed from other insects. Ongoing genomic sequencing efforts have revealed that most of these virus-derived entities are fully integrated into the genomes of parasitoid wasp lineages, representing endogenous viral elements (EVEs) that retain the ability to produce virus or virus-like particles within wasp reproductive tissues. All documented parasitoid EVEs have undergone similar genomic rearrangements compared to their viral ancestors characterized by viral genes scattered across wasp genomes and specific viral gene losses. The recurrent presence of viral endogenization and genomic reorganization in beneficial virus systems identified to date suggest that these features are crucial to forming heritable alliances between parasitoid wasps and viruses. Here, our genomic characterization of a mutualistic poxvirus associated with the wasp Diachasmimorpha longicaudata , known as Diachasmimorpha longicaudata entomopoxvirus (DlEPV), has uncovered the first instance of beneficial virus evolution that does not conform to the genomic architecture shared by parasitoid EVEs with which it displays evolutionary convergence. Rather, DlEPV retains the exogenous viral genome of its poxvirus ancestor and the majority of conserved poxvirus core genes. Additional comparative analyses indicate that DlEPV is related to a fly pathogen and contains a novel gene expansion that may be adaptive to its symbiotic role. Finally, differential expression analysis during virus replication in wasps and fly hosts demonstrates a unique mechanism of functional partitioning that allows DlEPV to persist within and provide benefit to its parasitoid wasp host. 

   more » « less
5. Genome and transcriptome mechanisms driving cephalopod evolution

   https://doi.org/10.1038/s41467-022-29748-w  

   Albertin, Caroline B. ; Medina-Ruiz, Sofia ; Mitros, Therese ; Schmidbaur, Hannah ; Sanchez, Gustavo ; Wang, Z. Yan ; Grimwood, Jane ; Rosenthal, Joshua J. C. ; Ragsdale, Clifton W. ; Simakov, Oleg ; et al ( May 2022 , Nature Communications)

   Cephalopods are known for their large nervous systems, complex behaviors and morphological innovations. To investigate the genomic underpinnings of these features, we assembled the chromosomes of the Boston market squid,Doryteuthis (Loligo) pealeii,and the California two-spot octopus,Octopus bimaculoides, and compared them with those of the Hawaiian bobtail squid,Euprymna scolopes. The genomes of the soft-bodied (coleoid) cephalopods are highly rearranged relative to other extant molluscs, indicating an intense, early burst of genome restructuring. The coleoid genomes feature multi-megabase, tandem arrays of genes associated with brain development and cephalopod-specific innovations. We find that a known coleoid hallmark, extensive A-to-I mRNA editing, displays two fundamentally distinct patterns: one exclusive to the nervous system and concentrated in genic sequences, the other widespread and directed toward repetitive elements. We conclude that coleoid novelty is mediated in part by substantial genome reorganization, gene family expansion, and tissue-dependent mRNA editing.

    

   more » « less