Anaerobic Sulfur Oxidation Underlies Adaptation of a Chemosynthetic Symbiont to Oxic-Anoxic Interfaces

Paredes, Gabriela F.; Viehboeck, Tobias; Lee, Raymond; Palatinszky, Márton; Mausz, Michaela A.; Reipert, Siegfried; Schintlmeister, Arno; Maier, Andreas; Volland, Jean-Marie; Hirschfeld, Claudia; Wagner, Michael; Berry, David; Markert, Stephanie; Bulgheresi, Silvia; König, Lena

doi:10.1128/msystems.01186-20

Cited by 11 publications

(26 citation statements)

References 170 publications

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“…To understand the molecular mechanisms underlying L. oneistus response to oxygen, we subjected it to various oxygen concentrations. Namely, nematode batches were incubated under either normoxic (100% air saturation; O), hypoxic (30% air saturation; H) or anoxic (0% air saturation; A) conditions for 24 h. Additionally, given that L. oneistus thrives in reduced sand containing up to 25 µM sulfide 16 , 17 , we also incubated it in anoxic seawater supplemented with < 25 µM sulfide (anoxic sulfidic condition; AS; see 16 for the sulfide concentration experienced by L. oneistus during each incubation).…”

Section: Resultsmentioning

confidence: 99%

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Differential regulation of degradation and immune pathways underlies adaptation of the ectosymbiotic nematode Laxus oneistus to oxic-anoxic interfaces

Paredes

Viehboeck

Markert

et al. 2022

Sci Rep

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Eukaryotes may experience oxygen deprivation under both physiological and pathological conditions. Because oxygen shortage leads to a reduction in cellular energy production, all eukaryotes studied so far conserve energy by suppressing their metabolism. However, the molecular physiology of animals that naturally and repeatedly experience anoxia is underexplored. One such animal is the marine nematode Laxus oneistus. It thrives, invariably coated by its sulfur-oxidizing symbiont Candidatus Thiosymbion oneisti, in anoxic sulfidic or hypoxic sand. Here, transcriptomics and proteomics showed that, whether in anoxia or not, L. oneistus mostly expressed genes involved in ubiquitination, energy generation, oxidative stress response, immune response, development, and translation. Importantly, ubiquitination genes were also highly expressed when the nematode was subjected to anoxic sulfidic conditions, together with genes involved in autophagy, detoxification and ribosome biogenesis. We hypothesize that these degradation pathways were induced to recycle damaged cellular components (mitochondria) and misfolded proteins into nutrients. Remarkably, when L. oneistus was subjected to anoxic sulfidic conditions, lectin and mucin genes were also upregulated, potentially to promote the attachment of its thiotrophic symbiont. Furthermore, the nematode appeared to survive oxygen deprivation by using an alternative electron carrier (rhodoquinone) and acceptor (fumarate), to rewire the electron transfer chain. On the other hand, under hypoxia, genes involved in costly processes (e.g., amino acid biosynthesis, development, feeding, mating) were upregulated, together with the worm’s Toll-like innate immunity pathway and several immune effectors (e.g., bactericidal/permeability-increasing proteins, fungicides). In conclusion, we hypothesize that, in anoxic sulfidic sand, L. oneistus upregulates degradation processes, rewires the oxidative phosphorylation and reinforces its coat of bacterial sulfur-oxidizers. In upper sand layers, instead, it appears to produce broad-range antimicrobials and to exploit oxygen for biosynthesis and development.

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Section: Resultsmentioning

confidence: 99%

“…Whereas transcriptional differences of the symbiont Candidatus Thiosymbion oneisti incubated under normoxic (O) and hypoxic (H) conditions were negligible 16 , the expression profiles of nematode batches incubated under O conditions varied so much that they did not cluster (Fig. S1 ).…”

Section: Resultsmentioning

confidence: 99%

Differential regulation of degradation and immune pathways underlies adaptation of the ectosymbiotic nematode Laxus oneistus to oxic-anoxic interfaces

Paredes

Viehboeck

Markert

et al. 2022

Sci Rep

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“…If, based on transcriptomics, Ca. T. oneisti might import phospholipids, ammonia, and organic compounds from its host and sulfide, oxygen, urea, and CO 2 from the environment ( Paredes et al., 2021 ), we still do not know which molecules Thiosymbion cells exchange among themselves. Therefore, the physiological needs that would drive the evolution of a cube-like cell await discovery.…”

Section: Discussionmentioning

confidence: 99%

FtsZ-mediated fission of a cuboid bacterial symbiont

et al. 2022

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Summary Less than a handful of cuboid and squared cells have been described in nature, which makes them a rarity. Here, we show how Candidatus Thiosymbion cuboideus, a cube-like gammaproteobacterium, reproduces on the surface of marine free-living nematodes. Immunostaining of symbiont cells with an anti-fimbriae antibody revealed that they are host-polarized, as these appendages exclusively localized at the host-proximal (animal-attached) pole. Moreover, by applying a fluorescently labeled metabolic probe to track new cell wall insertion in vivo , we observed that the host-attached pole started septation before the distal one. Similarly, Ca. T. cuboideus cells immunostained with an anti-FtsZ antibody revealed a proximal-to-distal localization pattern of this tubulin homolog. Although FtsZ has been shown to arrange into squares in synthetically remodeled cuboid cells, here we show that FtsZ may also mediate the division of naturally occurring ones. This implies that, even in natural settings, membrane roundness is not required for FtsZ function.

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“…A recent study showed an upregulation of transporter genes, indicating heterotrophy under oxic conditions in Cand. Thiosymbion oneisti, the thiotrophic ectosymbiont of the marine nematode Laxus oneistus [45]. Although genes that support this function are present in the metagenome assembled genome of Thiobius (Espada-Hinojosa pers.…”

Section: Plos Onementioning

confidence: 99%

Host-symbiont stress response to lack-of-sulfide in the giant ciliate mutualism

et al. 2022

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The mutualism between the thioautotrophic bacterial ectosymbiont Candidatus Thiobius zoothamnicola and the giant ciliate Zoothamnium niveum thrives in a variety of shallow-water marine environments with highly fluctuating sulfide emissions. To persist over time, both partners must reproduce and ensure the transmission of symbionts before the sulfide stops, which enables carbon fixation of the symbiont and nourishment of the host. We experimentally investigated the response of this mutualism to depletion of sulfide. We found that colonies released some initially present but also newly produced macrozooids until death, but in fewer numbers than when exposed to sulfide. The symbionts on the colonies proliferated less without sulfide, and became larger and more rod-shaped than symbionts from freshly collected colonies that were exposed to sulfide and oxygen. The symbiotic monolayer was severely disturbed by growth of other microbes and loss of symbionts. We conclude that the response of both partners to the termination of sulfide emission was remarkably quick. The development and the release of swarmers continued until host died and thus this behavior contributed to the continuation of the association.

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Anaerobic Sulfur Oxidation Underlies Adaptation of a Chemosynthetic Symbiont to Oxic-Anoxic Interfaces

Abstract: Chemoautotrophic endosymbionts are famous for exploiting sulfur oxidization to feed marine organisms with fixed carbon. However, the physiology of thiotrophic bacteria thriving on the surface of animals (ectosymbionts) is less understood.

Cited by 11 publications

References 170 publications

Differential regulation of degradation and immune pathways underlies adaptation of the ectosymbiotic nematode Laxus oneistus to oxic-anoxic interfaces

Differential regulation of degradation and immune pathways underlies adaptation of the ectosymbiotic nematode Laxus oneistus to oxic-anoxic interfaces

FtsZ-mediated fission of a cuboid bacterial symbiont

Host-symbiont stress response to lack-of-sulfide in the giant ciliate mutualism

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