Functional genomic analysis of an uncultured δ-proteobacterium in the sponge <i>Cymbastela concentrica</i>

Liu, Michael Yizhe; Kjelleberg, Staffan; Thomas, Torsten

doi:10.1038/ismej.2010.139

Cited by 50 publications

(38 citation statements)

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“…symbiont has been postulated to aid in attachment to the eukaryotic host and in avoidance of the host's immune response (Alex and Antunes, 2015). ANK-repeat proteins (ARPs) have been identified in abundance in the genomes of multiple sponge-associated bacteria (Liu et al, 2010;Thomas et al, 2010;Siegl et al, 2011;Fan et al, 2012;Hentschel et al, 2012;Tian et al, 2014;Alex and Antunes, 2015;Burgsdorf et al, 2015b;Britstein et al, 2016), including in the most dominant core symbiont of A. queenslandica, OTU 1, although not in OTU 4 (Gauthier et al, 2016). ARPs from bacterial symbionts have been experimentally shown to influence sponge-bacterial interactions, specifically via interfering with phagocytosis as a possible mechanism to escape digestion in a sponge host (Nguyen et al, 2014).…”

Section: Differential Expression Analysis Of Sponge Genes Indicates Smentioning

confidence: 99%

Ontogenetic Changes in the Bacterial Symbiont Community of the Tropical Demosponge Amphimedon queenslandica: Metamorphosis Is a New Beginning

et al. 2016

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Vertical transmission of bacterial symbionts, which is known in many species of sponge (Porifera), is expected to promote strong fidelity between the partners. Combining 16S rRNA gene amplicon sequencing and electron microscopy, we have assayed the relative abundance of vertically-inherited bacterial symbionts in several stages of the life cycle of Amphimedon queenslandica, a tropical coral reef sponge. We reveal that adult A. queenslandica house a low diversity microbiome dominated by just three proteobacterial OTUs, with a single gammaprotebacterium clearly dominant through much of the life cycle. This ontogenetic perspective has revealed that, although vertical transmission occurs very early in development, the inherited symbionts do not maintain proportional dominance of the bacterial community at every developmental stage. A reproductive bottleneck in the A. queenslandica life cycle is larval settlement, when a free-swimming pelagic larva settles out of the water column onto the benthos and completes metamorphoses into the sessile body plan within just 3-4 days. During this dramatic life cycle transition, an influx of environmentally-derived bacteria leads to a major reorganization of the microbiome, potentially challenging the fidelity and persistence of the vertically-inherited symbiotic relationships. However, dominance of the primary, vertically-inherited symbionts is restored in adult sponges. The mechanisms underlying ontogenetic changes in the bacterial community are unknown, including how the dominance of the primary symbionts is restored in the adult sponge-does the host or symbiont regulate this process? Using high-resolution transcriptional profiling in multiple stages of the A. queenslandica life cycle combined with this natural perturbation of the microbiome immediately following larval settlement, we are beginning to identify candidate host genes associated with animal-bacterial crosstalk. Among the sponge host genes upregulated during the times of active microbiome assembly, there is an enrichment of genes potentially involved in innate immunity, including scavenger receptors, and of genes containing eukaryote-like domains, which have elsewhere Fieth et al.Sponge Microbiome Changes through Lifecycle been implicated in host-symbiont interactions. Intriguingly, we also see an enrichment of sponge genes arising from ancient horizontal transfer events from bacteria, which raises the possibility that host-bacterial associations in the evolutionary past may help to regulate host-bacterial associations in the ecological present.

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Section: Differential Expression Analysis Of Sponge Genes Indicates Smentioning

confidence: 99%

Ontogenetic Changes in the Bacterial Symbiont Community of the Tropical Demosponge Amphimedon queenslandica: Metamorphosis Is a New Beginning

et al. 2016

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“…These are proteins with eukaryote-like domains, such as ankyrin repeats and tetratricopeptide repeats (TPR), which are likely to mediate protein-protein interactions (Siegl et al, 2011). The latter have been found in all known genomic datasets from prokaryotic sponge symbionts (Hallam et al, 2006;Liu, M., et al, 2011), and the expression of proteins with these domains has been confirmed . Ankyrins are especially likely to be of relevance as they might be involved in the recognition of and protection from host phagocytosis .…”

Section: Poribacterial Symbiont Of Marine Spongesmentioning

confidence: 90%

“…Degradation of complex substances was also suggested by Liu, M., et al (2011) for another bacterial symbiont of Cymbastella concentrica. Furthermore, Hallam et al (2006) reported on several proteases that might degrade extracellular matrix proteins as a defense mechanism on the genome of C. symbiosum in Axinella mexicana.…”

Section: Poribacterial Symbiont Of Marine Spongesmentioning

confidence: 95%

“…Similarly, metagenomics provided novel insights into chemoautotrophic symbioses, in that sulfuroxidizing and sulfate-reducing symbionts provide a gutless marine worm host with multiple sources of nutrition (Woyke et al, 2006). Moreover, omics approaches have provided the first glimpse into the functional gene repertoire of marine sponges and their beneficial microbial consortia (Hallam et al, 2006Liu, M., et al, 2011;Liu et al, 2012;Fan et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

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Exploring Symbioses by Single-Cell Genomics

Kamke

Bayer

Woyke

et al. 2012

The Biological Bulletin

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Abstract. Single-cell genomics has advanced the field of microbiology from the analysis of microbial metagenomes where information is "drowning in a sea of sequences," to recognizing each microbial cell as a separate and unique entity. Single-cell genomics employs Phi29 polymerasemediated whole-genome amplification to yield microgramrange genomic DNA from single microbial cells. This method has now been applied to a handful of symbiotic systems, including bacterial symbionts of marine sponges, insects (grasshoppers, termites), and vertebrates (mouse, human). In each case, novel insights were obtained into the functional genomic repertoire of the bacterial partner, which, in turn, led to an improved understanding of the corresponding host. Single-cell genomics is particularly valuable when dealing with uncultivated microorganisms, as is still the case for many bacterial symbionts. In this review, we explore the power of single-cell genomics for symbiosis research and highlight recent insights into the symbiotic systems that were obtained by this approach.

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“…They contribute to maintaining water clarity and to cycling nutrients between the water column and the sea floor (Bayer et al, 2008;Hallam et al, 2006;Hoffmann et al, 2009;Liu et al, 2010). These capabilities appear to be particularly important on tropical coral reefs, which typically exist in clear, nutrient-poor…”

Section: Introductionmentioning

confidence: 99%

Modelling sponge-symbiont metabolism

Watson¹

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Marine sponges are increasingly being recognised for their nutrient cycling ecosystem services, linking pelagic nutrients with the benthic ecosystem. Furthermore, sponges are the most prolific producers of bioactive secondary metabolites in the marine environment. Despite their ecological and commercial value, little is know about the metabolic processes that are responsible. The inability to produce sufficient sponge biomass, and thus specific bioactive compounds, has been repeatedly identified as a major bottleneck towards commercialising sponge holobiont derived drugs. Likewise, nutrient cycling by sponges has been a relatively recent advancement in marine ecology and the scale of this process is unknown. This thesis takes a systems approach to understanding sponge-symbiont metabolic processes by utilising the genomic resources available for the demosponge Amphimedon queenslandica and its bacterial symbiont AqS1. Specifically, I undertake genome-scale modelling and metabolic flux analyses to investigate the metabolic networks present in this sponge as well as its associated vertically-transmitted microbial symbiont. The goal of this thesis is to generate the data required for, and subsequently develop, a dual-species genome-scale metabolic model for A. queenslandica and AqS1. This will provide a framework to further our understanding of how sponges produce their biomass while living in an oligotrophic, tropical reef environment.To develop a genome-scale metabolic model, the biochemical composition of the organism must first be determined. Knowledge of the relative quantities of macromolecules and their respective building blocks (e.g. protein and amino acids) is vital, as each requires different substrates, enzymes and cofactors for their synthesis. I adapted and developed methods to characterise the composition and abundance of DNA, RNA, protein, lipids and carbohydrates in a marine sponge. These methods are described in detail that allows them to be easily transferred to other, non-model, large marine organisms. This is followed by a detailed analysis of A. queenslandica's macromolecular, amino acid, fatty acid and sterol composition. The biochemical data from this chapter was used to generate a biomass equation that represent the average composition of adult A. queenslandica in the metabolic model. 3To understand how the metabolic network may work towards producing more biomass, it must be considered in the context of the environmental conditions that naturally constrain growth. The dominant environmental constraint on growth on an oligotrophic reef system is nutrient availability.The abundance of key elements, such as carbon and nitrogen, were quantified throughout the course of a year. To investigate effects on the sponge of any changes in nutrient availability, I concurrently sampled sponges and analysed their biochemical composition to the macromolecular level. Chapter 4 presents these data and discusses a number of trends and correlations in the biochemical composition of the sponges with chan...

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Functional genomic analysis of an uncultured δ-proteobacterium in the sponge Cymbastela concentrica

Cited by 50 publications

References 54 publications

Ontogenetic Changes in the Bacterial Symbiont Community of the Tropical Demosponge Amphimedon queenslandica: Metamorphosis Is a New Beginning

Ontogenetic Changes in the Bacterial Symbiont Community of the Tropical Demosponge Amphimedon queenslandica: Metamorphosis Is a New Beginning

Exploring Symbioses by Single-Cell Genomics

Modelling sponge-symbiont metabolism

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