Transcriptomic and proteomic insights into innate immunity and adaptations to a symbiotic lifestyle in the gutless marine worm Olavius algarvensis

Wippler, Juliane; Kleiner, Manuel; Lott, Christian; Gruhl, Alexander; Abraham, Paul E.; Giannone, Richard J.; Young, J. C.; Hettich, Robert L.; Dubilier, Nicole

doi:10.1186/s12864-016-3293-y

Cited by 43 publications

(49 citation statements)

References 136 publications

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“…This system has benefited from some of the most sophisticated 'omics and visualization tools (Woyke et al, 2006). For example, multi-labeled probing has improved visualization of the microbiome (Schimak et al, 2016) and transcriptomics and proteomics have been applied to examine host-microbiome interactions, including energy transfer between the host and microbes (Kleiner et al, 2012) and recognition of the consortia by the worm's innate immune system (Wippler et al, 2016). The major strength of this system is that it does offer the ability to study host-microbiome interactions with a low diversity microbial consortium, and it also offers a number of host and microbial genomic resources (e.g., Woyke et al, 2006;Ruehland et al, 2008).…”

Section: Overview Of Diverse and Emerging Animal-microbiome Study Sysmentioning

confidence: 99%

Marine Animal Microbiomes: Toward Understanding Host–Microbiome Interactions in a Changing Ocean

2017

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All animals on Earth form associations with microorganisms, including protists, bacteria, archaea, fungi, and viruses. In the ocean, animal-microbial relationships were historically explored in single host-symbiont systems. However, new explorations into the diversity of microorganisms associating with diverse marine animal hosts is moving the field into studies that address interactions between the animal host and a more multi-member microbiome. The potential for microbiomes to influence the health, physiology, behavior, and ecology of marine animals could alter current understandings of how marine animals adapt to change, and especially the growing climate-related and anthropogenic-induced changes already impacting the ocean environment. This review explores the nature of marine animal-microbiome relationships and interactions, and possible factors that may shift associations from symbiotic to dissociated states. I present a brief review of current microbiome research and opportunities, using examples of select marine animals that span diverse phyla within the Animalia, including systems that are more and less developed for symbiosis research, including two represented in my own research program. Lastly, I consider challenges and emerging solutions for moving these and other study systems into a more detailed understanding of host-microbiome interactions within a changing ocean.

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Section: Overview Of Diverse and Emerging Animal-microbiome Study Sysmentioning

confidence: 99%

Marine Animal Microbiomes: Toward Understanding Host–Microbiome Interactions in a Changing Ocean

2017

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“…We detected a number of ‘symbiosis-specific’ Riftia proteins, which were co-enriched with symbiont cells in fractions XS and/or S and may thus facilitate direct host-microbe interactions or enable the host to provide optimal conditions for the symbiont. PGRPs, for example, are involved in innate immunity (Kang et al , 1998) and have previously been shown or suggested to participate in symbiotic interactions (Troll et al , 2009, Wang et al , 2009, Royet et al , 2011, Wippler et al , 2016). Since oxygen concentrations in the trophosome might be comparatively low (benefitting the microaerophilic symbionts; Hinzke et al , 2019), the hypoxia up-regulated Riftia proteins we detected may present a protective adaptation of the host to these hypoxic conditions.…”

Section: Discussionmentioning

confidence: 99%

Metabolic differences between symbiont subpopulations in the deep-sea tubewormRiftia pachyptila

Hinzke

Kleiner

Meister

et al. 2020

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The hydrothermal vent tube worm Riftia pachyptila lives in intimate symbiosis with intracellular sulfur-oxidizing gammaproteobacteria. Although the symbiont population consists of a single 16S rRNA phylotype, bacteria in the same host animal exhibit a remarkable degree of metabolic diversity: They simultaneously utilize two carbon fixation pathways and various energy sources and electron acceptors. Whether these multiple metabolic routes are employed in the same symbiont cells, or rather in distinct symbiont subpopulations, was unclear. As Riftia symbionts vary considerably in cell size and shape, we enriched individual symbiont cell sizes by density gradient centrifugation in order to test whether symbiont cells of different sizes show different metabolic profiles. Metaproteomic analysis and statistical evaluation using clustering and random forests, supported by microscopy and flow cytometry, strongly suggest that Riftia symbiont cells of different sizes represent metabolically dissimilar stages of a physiological differentiation process: Small symbionts actively divide and may establish cellular symbiont-host interaction, as indicated by highest abundance of the cell division key protein FtsZ and highly abundant chaperones and porins in this initial phase. Large symbionts, on the other hand, apparently do not divide, but still replicate DNA, leading to DNA endoreduplication. Highest abundance of enzymes for CO2 fixation, carbon storage and biosynthesis in large symbionts indicates that in this late differentiation stage the symbiont’s metabolism is efficiently geared towards the production of organic material. We propose that this division of labor between smaller and larger symbionts benefits the productivity of the symbiosis as a whole.

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“…All three microbiotypes found in this study were clearly defined by their bacterial community composition. This variability in bacterial community composition could result from multiple inter-organismal interactions such as hostspecific immune capacity allowing the presence or absence of bacteria incompatible with the presence of other bacterial genera [86][87][88][89]. These differences in microbial community composition, together with the systematic cooccurrence of certain bacterial taxa, create distinct functional biomarkers to the clam host.…”

Section: Microbiotypes In Giant Clamsmentioning

confidence: 99%

Metabarcoding reveals distinct microbiotypes in the giant clam Tridacna maxima

et al. 2020

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Background: Giant clams and scleractinian (reef-building) corals are keystone species of coral reef ecosystems. The basis of their ecological success is a complex and fine-tuned symbiotic relationship with microbes. While the effect of environmental change on the composition of the coral microbiome has been heavily studied, we know very little about the composition and sensitivity of the microbiome associated with clams. Here, we explore the influence of increasing temperature on the microbial community (bacteria and dinoflagellates from the family Symbiodiniaceae) harbored by giant clams, maintained either in isolation or exposed to other reef species. We created artificial benthic assemblages using two coral species (Pocillopora damicornis and Acropora cytherea) and one giant clam species (Tridacna maxima) and studied the microbial community in the latter using metagenomics. Results: Our results led to three major conclusions. First, the health status of giant clams depended on the composition of the benthic species assemblages. Second, we discovered distinct microbiotypes in the studied T. maxima population, one of which was disproportionately dominated by Vibrionaceae and directly linked to clam mortality. Third, neither the increase in water temperature nor the composition of the benthic assemblage had a significant effect on the composition of the Symbiodiniaceae and bacterial communities of T. maxima. Conclusions: Altogether, our results suggest that at least three microbiotypes naturally exist in the studied clam populations, regardless of water temperature. These microbiotypes plausibly provide similar functions to the clam host via alternate molecular pathways as well as microbiotype-specific functions. This redundancy in functions among microbiotypes together with their specificities provides hope that giant clam populations can tolerate some levels of environmental variation such as increased temperature. Importantly, the composition of the benthic assemblage could make clams susceptible to infections by Vibrionaceae, especially when water temperature increases.

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Transcriptomic and proteomic insights into innate immunity and adaptations to a symbiotic lifestyle in the gutless marine worm Olavius algarvensis

Cited by 43 publications

References 136 publications

Marine Animal Microbiomes: Toward Understanding Host–Microbiome Interactions in a Changing Ocean

Marine Animal Microbiomes: Toward Understanding Host–Microbiome Interactions in a Changing Ocean

Metabolic differences between symbiont subpopulations in the deep-sea tubewormRiftia pachyptila

Metabarcoding reveals distinct microbiotypes in the giant clam Tridacna maxima

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