Sponge-microbe partnerships are stable under eutrophication pressure from mariculture

Baquiran, Jake Ivan P.; Conaco, Cecilia

doi:10.1016/j.marpolbul.2018.09.011

Cited by 23 publications

(18 citation statements)

References 95 publications

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“…This mirrors findings from other studies in marine sponges that suggest that microbial communities are shaped by host identity (Chambers et al, 2013;Naim et al, 2014;Souza et al, 2016;Steinert et al, 2016). The sponge microbiome has been shown to be stable across individuals taken from different sampling locations or depths (Pita et al, 2013;Reveillaud et al, 2014) and can even withstand moderate pollution stress (Gantt, López-Legentil & Erwin, 2017;Baquiran & Conaco, 2018).…”

Section: Species Specificity Of Tetillid Sponge Prokaryotic Microbialsupporting

confidence: 84%

“…However, the stability of sponge microbial communities can vary among host species and under different environmental conditions. For example, the microbiomes of Cymbastela stipitata and Gelliodes obtusa remained stable even under eutrophication stress (Luter, Gibb & Webster, 2014;Baquiran & Conaco, 2018). Similarly, the microbiome of the Great Barrier Reef sponge, Rhopaloeides odorabile, did not change under eutrophication and elevated temperature conditions (Simister et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

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Population structure and microbial community diversity of two common tetillid sponges in a tropical reef lagoon

Baquiran

Nada

Posadas

et al. 2020

PeerJ

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Sponges are predicted to dominate future reef ecosystems influenced by anthropogenic stressors and global climate change. The ecological success of sponges is attributed to their complex physiology, which is in part due to the diversity of their associated prokaryotic microbiome. However, the lack of information on the microbial community of many sponge species makes it difficult to gauge their interactions and functional contributions to the ecosystem. Here, we investigated the population dynamics and microbial community composition of two tetillid sponges identified as Cinachyrella sp. and Paratetilla sp., which are common on coral bommies in a reef lagoon in Bolinao, northwestern Philippines. The sponges ranged in size from 2.75 ± 2.11 to 6.33 ± 3.98 cm (mean ± standard deviation) and were found at an average density of 1.57 ± 0.79 to 4.46 ± 3.60 individuals per sq. m. on the bommies. The tetillid sponge population structure remained stable over the course of four years of monitoring. Prokaryotic communities associated with the sponges were distinct but had overlapping functions based on PICRUSt2 predictions. This convergence of functions may reflect enrichment of metabolic processes that are crucial for the survival of the tetillid sponges under prevailing conditions in the reef lagoon. Differentially enriched functions related to carbon, sulfur, fatty acid, and amino acid metabolism, cellular defense, and stress response, may influence the interactions of tetillid sponges with other biota on the bommies.

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Section: Species Specificity Of Tetillid Sponge Prokaryotic Microbialsupporting

confidence: 84%

Section: Introductionmentioning

confidence: 99%

Population structure and microbial community diversity of two common tetillid sponges in a tropical reef lagoon

Baquiran

Nada

Posadas

et al. 2020

PeerJ

Self Cite

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“…Metamorphosis without attachment to substrate may be triggered by downregulation of cryptochrome genes under low light conditions (Jindrich et al., 2017). If this is the case, light attenuation due to high sedimentation load, particularly in reef areas heavily affected by fish farm effluents, could be a major factor affecting larval dispersal and settlement (Abdul Wahab, Maldonado, Luter, Jones, & Ricardo, 2019; Baquiran & Conaco, 2018; Quimpo et al., 2020). Alternatively, it is possible that larvae stay in the water column for much longer under dark conditions until they eventually encounter biochemical cues that have diffused from CCA.…”

Section: Discussionmentioning

confidence: 99%

“…Sponges, in particular, contribute to the structural complexity of the reef ecosystem and have important ecological roles, including the provision of habitats for various organisms and the recycling of nutrients from particulate and dissolved organic matter (Bell, 2008; Cabaitan, Gomez, & Yap, 2016; De Goeij et al., 2013; Diaz & Rützler, 2001). Sponges are hypothesized to be resilient to environmental stressors, with their abundance increasing on reefs affected by local anthropogenic stressors, recurrent bleaching events, and widespread habitat degradation (Baquiran & Conaco, 2018; Bell, Davy, Jones, Taylor, & Webster, 2013; Bell et al., 2015, 2018; Chaves‐Fonnegra et al, 2018). The recovery and persistence of marine sponge populations following disturbances are likely influenced by their reproductive strategies, larval supply, habitat selection, and successful recruitment (Abdul Wahab, de Nys, Abdo, Webster, & Whalan, 2014).…”

Section: Introductionmentioning

confidence: 99%

Behavior and development of larvae in the sponge Haliclona amboinensis

Nada

Baquiran

Cabaitan

et al. 2020

Invertebrate Biology

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Sponges play important roles in marine ecosystems by contributing to habitat complexity and benthopelagic coupling of nutrients. Yet, the reproduction and settlement behaviors of diverse sponge species are not well understood. Here, we examined the brooding demosponge Haliclona amboinensis, which is common on shallow reefs in Bolinao, northwestern Philippines. Gravid sponges were found between the months of May and August, coinciding with warmer sea surface temperature. Sponges released parenchymella larvae from brood chambers in the mid‐morning, suggesting that light and temperature may serve as cues to initiate hatching. Larvae immediately swam toward the surface upon emergence and migrated to the bottom of the tanks 1–2 hr after release. The presence of light and crustose coralline algae induced high larval settlement. Metamorphosis proceeded rapidly in vitro, with larval cells spreading laterally on the substrate. The osculum was first visible at 3 days after settlement. The short pelagic duration of larvae in H. amboinensis promotes local recruitment and may be important for the maintenance of sponge populations in the face of disturbances.

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“…However, T. wilhelma, H. panacea, and H. pigmentifera became stressed, sometimes fatally, during anoxia (16)(17)(18). Some marine sponge species also tolerate hypoxia and even anoxia in their natural environment (20)(21)(22)(23)(24), and gemmules from freshwater sponges can survive months of anoxia (25). Nevertheless, hypoxia-induced mortality was reported in situ for the demosponges Aaptos simplex and Homaxinella amphispicula (21), so responses are likely speciesspecific.…”

Section: Introductionmentioning

confidence: 99%

The effects of seasonal anoxia on the microbial community structure in demosponges in a marine lake (Lough Hyne, Ireland)

Schuster

Strehlow

Eckford-Soper

et al. 2020

Preprint

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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 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 semi-enclosed 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, though 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 distantly related hosts. We propose hypothetical host-symbiont interactions following deoxygenation that could confer deoxygenation tolerance.ImportanceThe 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 compared 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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Sponge-microbe partnerships are stable under eutrophication pressure from mariculture

Cited by 23 publications

References 95 publications

Population structure and microbial community diversity of two common tetillid sponges in a tropical reef lagoon

Population structure and microbial community diversity of two common tetillid sponges in a tropical reef lagoon

Behavior and development of larvae in the sponge Haliclona amboinensis

The effects of seasonal anoxia on the microbial community structure in demosponges in a marine lake (Lough Hyne, Ireland)

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