Bacterial diversity in the marine sponge<i>Halichondria panicea</i>from Icelandic waters and host-specificity of its dominant symbiont “<i>Candidatus</i>Halichondribacter symbioticus”

Knobloch, Stephen; Jóhannsson, Ragnar; Marteinsson, V.

doi:10.1093/femsec/fiy220

Cited by 56 publications

(50 citation statements)

References 76 publications

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“…Notwithstanding these potential anaerobic processes, the three symbiont combinations outlined above do not universally confer hypoxic tolerance to sponges in general but may be necessary for full anoxic tolerance. For example, Thaumarchaeota are effectively absent in the hypoxia-tolerant species H. panicea (92). Moreover, H. panicea contains high abundances (.75%) of an alphaproteobacterium as does its congeneric species Halichondria bowerbankii (Fig.…”

Section: Discussionmentioning

confidence: 99%

Effects of Seasonal Anoxia on the Microbial Community Structure in Demosponges in a Marine Lake in Lough Hyne, Ireland

Schuster

Strehlow

Eckford-Soper

et al. 2021

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Climate change is expanding marine oxygen minimum zones (OMZs), while anthropogenic nutrient input depletes oxygen concentrations locally. The effects of deoxygenation on animals are generally detrimental; however, some sponges (Porifera) exhibit hypoxic and anoxic tolerance through currently unknown mechanisms. Sponges harbor highly specific microbiomes, which can include microbes with anaerobic capabilities. Sponge-microbe symbioses must also have persisted through multiple anoxic/hypoxic periods throughout Earth’s history. Since sponges lack key components of the hypoxia-inducible factor (HIF) pathway responsible for hypoxic responses in other animals, it was hypothesized that sponge tolerance to deoxygenation may be facilitated by its microbiome. To test this hypothesis, we determined the microbial composition of sponge species tolerating seasonal anoxia and hypoxia in situ in a semienclosed marine lake, using 16S rRNA amplicon sequencing. We discovered a high degree of cryptic diversity among sponge species tolerating seasonal deoxygenation, including at least nine encrusting species of the orders Axinellida and Poecilosclerida. Despite significant changes in microbial community structure in the water, sponge microbiomes were species specific and remarkably stable under varied oxygen conditions, which was further explored for Eurypon spp. 2 and Hymeraphia stellifera. However, some symbiont sharing occurred under anoxia. At least three symbiont combinations, all including large populations of Thaumarchaeota, corresponded with deoxygenation tolerance, and some combinations were shared between some distantly related hosts. We propose hypothetical host-symbiont interactions following deoxygenation that could confer deoxygenation tolerance. IMPORTANCE The oceans have an uncertain future due to anthropogenic stressors and an uncertain past that is becoming clearer with advances in biogeochemistry. Both past and future oceans were, or will be, deoxygenated in comparison to present conditions. Studying how sponges and their associated microbes tolerate deoxygenation provides insights into future marine ecosystems. Moreover, sponges form the earliest branch of the animal evolutionary tree, and they likely resemble some of the first animals. We determined the effects of variable environmental oxygen concentrations on the microbial communities of several demosponge species during seasonal anoxia in the field. Our results indicate that anoxic tolerance in some sponges may depend on their symbionts, but anoxic tolerance was not universal in sponges. Therefore, some sponge species could likely outcompete benthic organisms like corals in future, reduced-oxygen ecosystems. Our results support the molecular evidence that sponges and other animals have a Neoproterozoic origin and that animal evolution was not limited by low-oxygen conditions.

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Section: Discussionmentioning

confidence: 99%

Effects of Seasonal Anoxia on the Microbial Community Structure in Demosponges in a Marine Lake in Lough Hyne, Ireland

Schuster

Strehlow

Eckford-Soper

et al. 2021

mSphere

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“…We explored both the repertoire and gene expression patterns of PRRs, as well as the induced immune response to bacterial LPS. H. panicea is an LMA sponge and is dominated by an extracellular alphaproteobacterial symbiont that is unique to this sponge species ( 32 , 33 ). Our results provide a first understanding on the innate immune system of H. panicea in the context of sponge-microbe interactions.…”

Section: Introductionmentioning

confidence: 99%

Individuality in the Immune Repertoire and Induced Response of the Sponge Halichondria panicea

2021

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The animal immune system mediates host-microbe interactions from the host perspective. Pattern recognition receptors (PRRs) and the downstream signaling cascades they induce are a central part of animal innate immunity. These molecular immune mechanisms are still not fully understood, particularly in terms of baseline immunity vs induced specific responses regulated upon microbial signals. Early-divergent phyla like sponges (Porifera) can help to identify the evolutionarily conserved mechanisms of immune signaling. We characterized both the expressed immune gene repertoire and the induced response to lipopolysaccharides (LPS) in Halichondria panicea, a promising model for sponge symbioses. We exposed sponges under controlled experimental conditions to bacterial LPS and performed RNA-seq on samples taken 1h and 6h after exposure. H. panicea possesses a diverse array of putative PRRs. While part of those PRRs was constitutively expressed in all analyzed sponges, the majority was expressed individual-specific and regardless of LPS treatment or timepoint. The induced immune response by LPS involved differential regulation of genes related to signaling and recognition, more specifically GTPases and post-translational regulation mechanisms like ubiquitination and phosphorylation. We have discovered individuality in both the immune receptor repertoire and the response to LPS, which may translate into holobiont fitness and susceptibility to stress. The three different layers of immune gene control observed in this study, - namely constitutive expression, individual-specific expression, and induced genes -, draw a complex picture of the innate immune gene regulation in H. panicea. Most likely this reflects synergistic interactions among the different components of immunity in their role to control and respond to a stable microbiome, seawater bacteria, and potential pathogens.

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“…Although these OTUs could be found in other biotopes, they were particularly abundant in each of these species. Previous studies have shown that LMA sponges tend to be dominated by distinct subsets of highly abundant OTUs and sometimes even a single dominant OTU, in addition to sharing a large amount of OTUs with seawater samples (Cleary et al., 2015, 2018; Croué et al., 2013; Giles et al., 2013; Knobloch et al., 2018; de Voogd et al., 2015). Our results thus suggest LMA status for the species Svenzea novo sp., P .…”

Section: Discussionmentioning

confidence: 99%

Composition and diversity of prokaryotic communities sampled from sponges and soft corals in Maldivian waters

2021

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Coral reefs are one of the most productive and diverse marine ecosystems on the planet and harbour a wide array of taxa including hard and soft corals, sponges, fishes and other invertebrate species. In addition to these large taxa, coral reefs also provide habitat for a range of distinct microbial communities in the abiotic environment (seawater and sediment) and living in symbiosis with the above-mentioned

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Bacterial diversity in the marine spongeHalichondria paniceafrom Icelandic waters and host-specificity of its dominant symbiont “CandidatusHalichondribacter symbioticus”

Cited by 56 publications

References 76 publications

Effects of Seasonal Anoxia on the Microbial Community Structure in Demosponges in a Marine Lake in Lough Hyne, Ireland

Effects of Seasonal Anoxia on the Microbial Community Structure in Demosponges in a Marine Lake in Lough Hyne, Ireland

Individuality in the Immune Repertoire and Induced Response of the Sponge Halichondria panicea

Composition and diversity of prokaryotic communities sampled from sponges and soft corals in Maldivian waters

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