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Gould, A. L.

Publications and source records attributed to Gould, A. L..

5 recordsLinked to original sources

High specificity meets genomic flexibility in the Siphamia-Photobacterium symbiosis

Host-microbe symbioses must balance partner specificity with enough flexibility to remain adaptable to environmental change. The Siphamia-Photobacterium symbiosis exemplifies this balance, as tropical siphonfish (Siphamia spp.) form a highly specific association with the bioluminescent bacterium Photobacterium mandapamensis, though it is unknown whether this specificity extends to temperate species of siphonfish. Here, we use long-read genome sequencing and functional assays to characterize the strain-level diversity of symbionts isolated from two temperate siphonfish hosts, Siphamia cephalotes and Siphamia roseigaster, and compare them to tropical isolates. We found that both hosts exclusively associate with P. mandapamensis in their light organs and that temperate strains form host-specific clades despite being collected in close proximity (< 5km). This is consistent with selective host filtering, microhabitat-driven adaptation, or conspecific host seeding. Pangenome analyses showed notable differences in accessory gene content, variation in the lux-rib operon, and a dramatic expansion of mobile genetic element (MGE) content in a subset of strains. We also identified the first host-derived P. mandapamensis isolate that is non-luminescent under laboratory conditions despite an intact lux-rib operon. Luminescence varied across strains, salinities, and temperature but was not correlated with the presence of luxF, with the majority of high-MGE strains exhibiting reduced light output. Together, these results extend the specificity of the Siphamia-Photobacterium symbiosis into temperate hosts and show that animals can maintain tight symbiont specificity despite the symbiont harboring substantial genomic and phenotypic flexibility at the strain level.

microbiology↗

Priority Effects Can Shape Strain-Level Community Assembly and Function in a Bioluminescent Symbiosis

Symbiotic microbial communities often appear highly variable in their composition and function in ways that environmental factors alone cannot explain. One potential reason for this variability is priority effects, where historical contingency in arrival order affects how symbionts assemble into communities. Focusing on the luminous bacterium (Photobacterium mandapamensis) in the light organ of the sea urchin cardinalfish (Siphamia tubifer), we studied how priority effects might influence bacterial symbiont assembly. In in vitro experiments that used three P. mandapamensis strains isolated from the same individual fish, we found that whichever strain arrived first dominated over the other two strains, indicating strong priority effects. We also found that the strains differed in growth and luminosity, and that the bioluminescence of the three-strain community could not be predicted from individual strain performances. These findings suggest that priority effects can be a major process shaping the composition and function of these symbiotic microbial communities.

ecology↗

Chromosomal-level genome assembly of the bioluminescent cardinalfishSiphamia tubifer, an emerging model for symbiosis research

The bioluminescent symbiosis between the sea urchin cardinalfish Siphamia tubifer (Kurtiformes: Apogonidae) and the luminous bacterium Photobacterium mandapamensis is an emerging vertebrate-bacteria model for the study of microbial symbiosis. However, there is little genetic data available for the host fish, limiting the scope of potential research that can be carried out with this association. In this study, we present a chromosomal-level genome assembly of S. tubifer using a combination of PacBio HiFi sequencing and Hi-C technologies. The final genome assembly was 1.2 Gb distributed on 23 chromosomes and contained 32,365 protein coding genes with a BUSCO completeness score of 99%. A comparison of the S. tubifer genome to that of another non-luminous cardinalfish revealed a high degree of synteny, whereas a similar comparison to a more distant relative in the Gobiiformes order revealed a fusion of two chromosomes in the cardinalfish genomes. An additional comparison of orthologous clusters among these three genomes revealed a set of 710 clusters that were unique to S. tubifer in which 23 GO pathways were significantly enriched, including several relating to host-microbe interactions and one involved in visceral muscle development, which could be related to the musculature involved in the gut-associated light organ of S. tubifer. We also assembled the complete mitogenome of S. tubifer and discovered both an inversion in the WANCY tRNA gene region resulting in a WACNY gene order as well as heteroplasmy in the length of the control region for this individual. A phylogenetic analysis based on the whole mitochondrial genome indicated that S. tubifer is divergent from the rest of the cardinalfish family, bringing up questions of the involvement of the bioluminescent symbiosis in the initial divergence of the ancestral Siphamia species. This draft genome assembly of S. tubifer will enable future studies investigating the evolution of bioluminescence in fishes as well as candidate genes involved in the symbiosis and will provide novel opportunities to use this system as a vertebrate-bacteria model for symbiosis research.

genomics↗

Population genomics of a bioluminescent symbiosis sheds light on symbiont transmission and specificity

All organisms depend on symbiotic associations with bacteria for their success, yet the processes by which specific symbioses are established and persist remain largely undescribed. To examine the ecological mechanisms involved in maintaining symbiont specificity over host generations, we examined the population genomics of a binary symbiosis involving the coral reef cardinalfish Siphamia tubifer and the luminous bacterium Photobacterium mandapamensis. Using restriction site-associated sequencing (RAD-Seq) methods we demonstrate that the facultative symbiont of S. tubifer exhibits genetic structure at spatial scales of tens of kilometers in Okinawa, Japan in the absence of physical dispersal barriers and in contrast to the host fish. These results suggest the hosts behavioral ecology help structure symbiont populations at a reef site by symbiont enrichment, consequently fostering symbiont specificity. This approach also revealed several symbiont genes that were divergent between host populations including genes known to play a role in other host-bacteria associations.

ecology↗

High-dimensional microbiome interactions shape host fitness

Gut bacteria can affect key aspects of host fitness, such as development, fecundity, and lifespan, while the host in turn shapes the gut microbiome. Microbiomes co-evolve with their hosts and have been implicated in host speciation. However, it is unclear to what extent individual species versus community interactions within the microbiome are linked to host fitness. Here we combinatorially dissect the natural microbiome of Drosophila melanogaster and reveal that interactions between bacteria shape host fitness through life history tradeoffs. We find that the same microbial interactions that shape host fitness also shape microbiome abundances, suggesting a potential evolutionary mechanism by which microbiome communities (rather than just individual species) may be intertwined in co-selection with their hosts. Empirically, we made germ-free flies colonized with each possible combination of the five core species of fly gut bacteria. We measured the resulting bacterial community abundances and fly fitness traits including development, reproduction, and lifespan. The fly gut promoted bacterial diversity, which in turn accelerated development, reproduction, and aging: flies that reproduced more died sooner. From these measurements we calculated the impact of bacterial interactions on fly fitness by adapting the mathematics of genetic epistasis to the microbiome. Host physiology phenotypes were highly dependent on interactions between bacterial species. Higher-order interactions (involving 3, 4, and 5 species) were widely prevalent and impacted both host physiology and the maintenance of gut diversity. The parallel impacts of bacterial interactions on the microbiome and on host fitness suggest that microbiome interactions may be key drivers of evolution.\n\nSignificanceAll animals have associated microbial communities called microbiomes that can influence the physiology and fitness of their host. It is unclear to what extent individual microbial species versus ecology of the microbiome influences fitness of the host. Here we mapped all the possible interactions between individual species of bacteria with each other and with the hosts physiology. Our approach revealed that the same bacterial interactions that shape microbiome abundances also shape host fitness traits. This relationship provides a feedback that may favor the emergence of co-evolving microbiome-host units.

microbiology↗