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Endosymbiont genomes yield clues of tubeworm success.

ABSTRACT: Forty years after discovery of chemosynthetic symbiosis in the tubeworm Riftia pachyptila, how organisms maintain their unique host-symbiont associations at the cellular level is still largely unknown. Previous studies primarily focus on symbionts associated with host lineages living in hydrothermal vents. To understand physiological adaptations and evolution in these holobiont systems in markedly different habitats, we characterized four novel siboglinid-symbiont genomes spanning deep-sea seep and sedimented environments. Our comparative analyses suggest that all sampled siboglinid chemoautotrophic symbionts, except for frenulate symbionts, can use both rTCA and Calvin cycle for carbon fixation. We hypothesize that over evolutionary time siboglinids have been able to utilize different bacterial lineages allowing greater metabolic flexibility of carbon fixation (e.g., rTCA) enabling tubeworms to thrive in more reducing habitats, such as vents and seeps. Moreover, we show that sulfur metabolism and molecular mechanisms related to initial infection are remarkably conserved across chemoautotrophic symbionts in different habitats. Unexpectedly, we find that the ability to use hydrogen, as an additional energy source, is potentially more widespread than previously recognized. Our comparative genomic results help elucidate potential mechanisms used to allow chemosynthetically dependent holobionts adapt to, and evolve in, different environments.

SUBMITTER: Li Y

PROVIDER: S-EPMC6194059 | biostudies-literature | 2018 Nov

REPOSITORIES: biostudies-literature

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Endosymbiont genomes yield clues of tubeworm success.

Li Yuanning Y Liles Mark R MR Halanych Kenneth M KM

The ISME journal 20180718 11

Forty years after discovery of chemosynthetic symbiosis in the tubeworm Riftia pachyptila, how organisms maintain their unique host-symbiont associations at the cellular level is still largely unknown. Previous studies primarily focus on symbionts associated with host lineages living in hydrothermal vents. To understand physiological adaptations and evolution in these holobiont systems in markedly different habitats, we characterized four novel siboglinid-symbiont genomes spanning deep-sea seep ...[more]

PMID: 30022157

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Project description:BackgroundThe endosymbiont Wolbachia pipientis infects a broad range of arthropod and filarial nematode hosts. These diverse associations form an attractive model for understanding host:symbiont coevolution. Wolbachia's ubiquity and ability to dramatically alter host reproductive biology also form the foundation of research strategies aimed at controlling insect pests and vector-borne disease. The Wolbachia strains that infect nematodes are phylogenetically distinct, strictly vertically transmitted, and required by their hosts for growth and reproduction. Insects in contrast form more fluid associations with Wolbachia. In these taxa, host populations are most often polymorphic for infection, horizontal transmission occurs between distantly related hosts, and direct fitness effects on hosts are mild. Despite extensive interest in the Wolbachia system for many years, relatively little is known about the molecular mechanisms that mediate its varied interactions with different hosts. We have compared the genomes of the Wolbachia that infect Drosophila melanogaster, wMel and the nematode Brugia malayi, wBm to that of an outgroup Anaplasma marginale to identify genes that have experienced diversifying selection in the Wolbachia lineages. The goal of the study was to identify likely molecular mechanisms of the symbiosis and to understand the nature of the diverse association across different hosts.ResultsThe prevalence of selection was far greater in wMel than wBm. Genes contributing to DNA metabolism, cofactor biosynthesis, and secretion were positively selected in both lineages. In wMel there was a greater emphasis on DNA repair, cell division, protein stability, and cell envelope synthesis.ConclusionSecretion pathways and outer surface protein encoding genes are highly affected by selection in keeping with host:parasite theory. If evidence of selection on various cofactor molecules reflects possible provisioning, then both insect as well as nematode Wolbachia may be providing substances to hosts. Selection on cell envelope synthesis, DNA replication and repair machinery, heat shock, and two component switching suggest strategies insect Wolbachia may employ to cope with diverse host and intra-host environments.

Project description:Cell physiology in the weevil Sitophilus oryzae is coordinated by three integrated genomes: nuclear, mitochondrial, and the "S. oryzae principal endosymbiont" (SOPE). SOPE, a cytoplasmic bacterium (2 x 10(3) bacteria per specialized bacteriocyte cell and 3 x 10(6) bacteria per weevil) that belongs to the proteobacteria gamma3-subgroup, is present in all weevils studied. We discovered a fourth prokaryotic genome in somatic and germ tissues of 57% of weevil strains of three species, S. oryzae, Sitophilus zeamais, and Sitophilus granarius, distributed worldwide. We assigned this Gram-negative prokaryote to the Wolbachia group (alpha-proteobacteria), on the basis of 16S rDNA sequence and fluorescence in situ DNA-RNA hybridization (FISH). Both bacteria, SOPE and Wolbachia, were selectively eliminated by combined heat and antibiotic treatments. Study of bacteria involvement in this insect's genetics and physiology revealed that SOPE, which induces the specific differentiation of the bacteriocytes, increases mitochondrial oxidative phosphorylation through the supply of pantothenic acid and riboflavin. Elimination of this gamma3-proteobacterium impairs many physiological traits. By contrast, neither the presence nor the absence of Wolbachia significantly affects the weevil's physiology. Wolbachia, disseminated throughout the body cells, is in particularly high density in the germ cells, where it causes nucleocytoplasmic incompatibility. The coexistence of two distinct types of intracellular proteobacteria at different levels of symbiont integration in insects illustrates the genetic complexity of animal tissue. Furthermore, evolutionary timing can be inferred: first nucleocytoplasm, then mitochondria, then SOPE, and finally Wolbachia. Symbiogenesis, the genetic integration of long-term associated members of different species, in the weevil appears to be a mechanism of speciation (with Wolbachia) and provides a means for animals to acquire new genes that permit better adaptation to the environment (with SOPE).

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Endosymbiont genomes yield clues of tubeworm success.

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Endosymbiont genomes yield clues of tubeworm success.

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