Sara Campana

University of Amsterdam

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Jasper M. de Goeij

University of Amsterdam

Manuel Aranda

King Abdullah University of Science and Technology

Gerard Muyzer

University of Amsterdam

Sebastian Schmidt‐Roach

King Abdullah University of Science and Technology

Maha J. Cziesielski

King Abdullah University of Science and Technology

Guoxin Cui

King Abdullah University of Science and Technology

Ana Riesgo

Museo Nacional de Ciencias Naturales

Yi Jin Liew

Royal Botanic Garden Edinburgh

Evelien Jongepier

University of Münster

Shannon G. Klein

King Abdullah University of Science and Technology

Cooperative Institutions

University of Amsterdam

King Abdullah University of Science and Technology

Google (United States)

Royal Netherlands Institute for Sea Research

Utrecht University

University of Florence

Clinical Research Center Kiel

Red Sea University

Consejo Superior de Investigaciones Científicas

Kiel University

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Multi-omics analysis of thermal stress response in a zooxanthellate cnidarian reveals the importance of associating with thermotolerant symbionts

Proceedings of the Royal Society B Biological Sciences (2018)

Maha J. Cziesielski Yi Jin Liew Guoxin Cui Sebastian Schmidt‐Roach Sara Campana

Corals and their endosymbiotic dinoflagellates of the genus Symbiodinium have a fragile relationship that breaks down under heat stress, an event known as bleaching. However, many coral species have adapted to high temperature environments such as the Red Sea (RS). To investigate mechanisms underlying temperature adaptation in zooxanthellate cnidarians we compared transcriptome- and proteome-wide heat stress response (24 h at 32°C) of three strains of the model organism Aiptasia pallida from regions with differing temperature profiles; North Carolina (CC7), Hawaii (H2) and the RS. Correlations between transcript and protein levels were generally low but inter-strain comparisons highlighted a common core cnidarian response to heat stress, including protein folding and oxidative stress pathways. RS anemones showed the strongest increase in antioxidant gene expression and exhibited significantly lower reactive oxygen species (ROS) levels in hospite . However, comparisons of antioxidant gene and protein expression between strains did not show strong differences, indicating similar antioxidant capacity across the strains. Subsequent analysis of ROS production in isolated symbionts confirmed that the observed differences of ROS levels in hospite were symbiont-driven. Our findings indicate that RS anemones do not show increased antioxidant capacity but may have adapted to higher temperatures through association with more thermally tolerant symbionts.

Anthozoa

Symbiodinium

Proteome

Coral bleaching

10.1098/rspb.2017.2654

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Processing of Naturally Sourced Macroalgal- and Coral-Dissolved Organic Matter (DOM) by High and Low Microbial Abundance Encrusting Sponges

Frontiers in Marine Science (2021)

Sara Campana Meggie Hudspith David Lankes Anna de Kluijver Celine Demey

Sponges play a key role in (re)cycling of dissolved organic matter (DOM) and inorganic nutrients in coral reef ecosystems. Macroalgae and corals release different quantities of DOM and at different bioavailabilities to sponges and their microbiome. Given the current coral- to algal-dominance shift on coral reefs, we assessed the differential processing of macroalgal- and coral-DOM by three high and three low microbial abundance (HMA and LMA) encrusting sponge species. We followed the assimilation of naturally sourced 13 C- and 15 N-enriched macroalgal- and coral-DOM into bulk tissue and into host- versus bacteria-specific phospholipid fatty acids (PLFAs). Additionally, we compared sponge-processing of the two natural DOM sources with 13 C- and 15 N-enriched laboratory-made diatom-DOM. All investigated sponges utilized all DOM sources, with higher assimilation rates in LMA compared to HMA sponges. No difference was found in carbon assimilation of coral- versus macroalgal-DOM into bulk tissue and host- versus bacteria-specific PLFAs, but macroalgal nitrogen was assimilated into bulk tissue up to eight times faster compared to the other sources, indicating its higher bioavailability to the sponges. Additionally, LMA sponges released significantly more inorganic nitrogen after feeding on macroalgal-DOM. Therefore, we hypothesize that, depending on the abundance and composition of the sponge community, sponges could catalyze reef eutrophication through increased turnover of nitrogen under coral-to-algal regime shifts.

Sponge

10.3389/fmars.2021.640583

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DNA ‐stable isotope probing (DNA‐SIP) identifies marine sponge‐associated bacteria actively utilizing dissolved organic matter (DOM)

Environmental Microbiology (2021)

Sara Campana Kathrin Busch Ute Hentschel Gerard Muyzer Jasper M. de Goeij

Sponges possess exceptionally diverse associated microbial communities and play a major role in (re)cycling of dissolved organic matter (DOM) in marine ecosystems. Linking sponge-associated community structure with DOM utilization is essential to understand host-microbe interactions in the uptake, processing, and exchange of resources. We coupled, for the first time, DNA-stable isotope probing (DNA-SIP) with 16S rRNA amplicon sequencing in a sponge holobiont to identify which symbiotic bacterial taxa are metabolically active in DOM uptake. Parallel incubation experiments with the sponge Plakortis angulospiculatus were amended with equimolar quantities of unlabelled (12 C) and labelled (13 C) DOM. Seven bacterial amplicon sequence variants (ASVs), belonging to the phyla PAUC34f, Proteobacteria, Poribacteria, Nitrospirae, and Chloroflexi, were identified as the first active consumers of DOM. Our results support the predictions that PAUC34f, Poribacteria, and Chloroflexi are capable of organic matter degradation through heterotrophic carbon metabolism, while Nitrospirae may have a potential mixotrophic metabolism. We present a new analytical application of DNA-SIP to detect substrate incorporation into a marine holobiont with a complex associated bacterial community and provide new experimental evidence that links the identity of diverse sponge-associated bacteria to the consumption of DOM.

Stable-isotope probing

Sponge

10.1111/1462-2920.15642

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Citations (33)

Meta-transcriptomic comparison of two sponge holobionts feeding on coral- and macroalgal-dissolved organic matter

BMC Genomics (2022)

Sara Campana Ana Riesgo Evelien Jongepier Janina Fuß Gerard Muyzer

Sponge holobionts (i.e., the host and its associated microbiota) play a key role in the cycling of dissolved organic matter (DOM) in marine ecosystems. On coral reefs, an ecological shift from coral-dominated to algal-dominated ecosystems is currently occurring. Given that benthic corals and macroalgae release different types of DOM, in different abundances and with different bioavailability to sponge holobionts, it is important to understand how the metabolic activity of the host and associated microbiota change in response to the exposure to both DOM sources. Here, we look at the differential gene expression of two sponge holobionts 6 hours after feeding on naturally sourced coral- and macroalgal-DOM using RNA sequencing and meta-transcriptomic analysis.We found a slight, but significant differential gene expression in the comparison between the coral- and macroalgal-DOM treatments in both the high microbial abundance sponge Plakortis angulospiculatus and the low microbial abundance sponge Haliclona vansoesti. In the hosts, processes that regulate immune response, signal transduction, and metabolic pathways related to cell proliferation were elicited. In the associated microbiota carbohydrate metabolism was upregulated in both treatments, but coral-DOM induced further lipid and amino acids biosynthesis, while macroalgal-DOM caused a stress response. These differences could be driven by the presence of distinct organic macronutrients in the two DOM sources and of small pathogens or bacterial virulence factors in the macroalgal-DOM.This work provides two new sponge meta-transcriptomes and a database of putative genes and genetic pathways that are involved in the differential processing of coral- versus macroalgal-DOM as food source to sponges with high and low abundances of associated microbes. These pathways include carbohydrate metabolism, signaling pathways, and immune responses. However, the differences in the meta-transcriptomic responses of the sponge holobionts after 6 hours of feeding on the two DOM sources were small. Longer-term responses to both DOM sources should be assessed to evaluate how the metabolism and the ecological function of sponges will be affected when reefs shift from coral towards algal dominance.

Sponge

Holobiont

Keystone species

10.1186/s12864-022-08893-y

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Citations (5)

Supplemental Dataset S1 from Multi-omics analysis of thermal stress response in a zooxanthellate cnidarian reveals the importance of associating with thermotolerant symbionts

Figshare (2018)

Maha J. Cziesielski Yi Jin Liew Guoxin Cui Sebastian Schmidt‐Roach Sara Campana

All significant GO Terms enriched for RS transcriptome

10.6084/m9.figshare.6057104

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Citations (0)

Additional file 1 of Meta-transcriptomic comparison of two sponge holobionts feeding on coral- and macroalgal-dissolved organic matter

Figshare (2022)

Sara Campana Ana Riesgo Evelien Jongepier Janina Fuß Gerard Muyzer

Additional file 1.

Sponge

10.6084/m9.figshare.21251756

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Additional file 2 of Meta-transcriptomic comparison of two sponge holobionts feeding on coral- and macroalgal-dissolved organic matter

Figshare (2022)

Sara Campana Ana Riesgo Evelien Jongepier Janina Fuß Gerard Muyzer

Additional file 2.

Sponge

10.6084/m9.figshare.21251762

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Local adaptation moderates the response of a cnidarian symbiosis to warming

Marcela Herrera Sarrias Shannon G. Klein Sebastian Schmidt‐Roach Sara Campana Maha J. Cziesielski

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Harnessing solar power: photoautotrophy supplements the diet of a low-light dwelling sponge

The ISME Journal (2022)

Meggie Hudspith Jasper M. de Goeij Mischa Streekstra Niklas A. Kornder Jeremy Bougoure

Abstract The ability of organisms to combine autotrophy and heterotrophy gives rise to one of the most successful nutritional strategies on Earth: mixotrophy. Sponges are integral members of shallow-water ecosystems and many host photosynthetic symbionts, but studies on mixotrophic sponges have focused primarily on species residing in high-light environments. Here, we quantify the contribution of photoautotrophy to the respiratory demand and total carbon diet of the sponge Chondrilla caribensis, which hosts symbiotic cyanobacteria and lives in low-light environments. Although the sponge is net heterotrophic at 20 m water depth, photosynthetically fixed carbon potentially provides up to 52% of the holobiont’s respiratory demand. When considering the total mixotrophic diet, photoautotrophy contributed an estimated 7% to total daily carbon uptake. Visualization of inorganic 13C- and 15N-incorporation using nanoscale secondary ion mass spectrometry (NanoSIMS) at the single-cell level confirmed that a portion of nutrients assimilated by the prokaryotic community was translocated to host cells. Photoautotrophy can thus provide an important supplemental source of carbon for sponges, even in low-light habitats. This trophic plasticity may represent a widespread strategy for net heterotrophic sponges hosting photosymbionts, enabling the host to buffer against periods of nutritional stress.

Mixotroph

Autotroph

Sponge

10.1038/s41396-022-01254-3

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Citations (15)

Marine sponges maintain stable bacterial communities between reef sites with different coral to algae cover ratios

FEMS Microbiology Ecology (2021)

Sara Campana Celine Demey Kathrin Busch Ute Hentschel Gerard Muyzer

Marine sponges play a major ecological role in recycling resources on coral reef ecosystems. The cycling of resources may largely depend on the stability of the host-microbiome interactions and their susceptibility to altered environmental conditions. Given the current coral to algal phase shift on coral reefs, we investigated whether the sponge-associated bacterial communities of four sponge species, with either high or low microbial abundances (HMA and LMA), remain stable at two reefs sites with different coral to algae cover ratios. Additionally, we assessed the bacterial community composition of two of these sponge species before and after a reciprocal transplantation experiment between the sites. An overall stable bacterial community composition was maintained across the two sites in all sponge species, with a high degree of host-specificity. Furthermore, the core bacterial communities of the sponges remained stable also after a 21-day transplantation period, although a minor shift was observed in less abundant taxa (< 1%). Our findings support the conclusion that host identity and HMA-LMA status are stronger traits in shaping bacterial community composition than habitat. Nevertheless, long-term microbial monitoring of sponges along with benthic biomass and water quality assessments are needed for identifying ecosystem tolerance ranges and tipping points in ongoing coral reef phase shifts.

Marine ecosystem

10.1093/femsec/fiab115

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Citations (12)