Sponge-Microbe Associations Survive High Nutrients and Temperatures

Simister, Rachel L.; Taylor, Michael W.; Tsai, Peter; Webster, Nicole S.

doi:10.1371/journal.pone.0052220

Cited by 74 publications

(52 citation statements)

References 115 publications

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“…Together, these results suggest a context dependency in either the composition of the active members of the sponge microbiome or in sponge‐microbial interactions (Fiore et al ; Maldonado et al ; Thacker and Freeman ). Traditionally the microbial community within sponges has been considered spatially and temporally stable (Erwin et al ; Simister et al ). However, recent work has shown that the active members of sponges' microbial communities can change, sometimes over short temporal scales (Zhang et al ; Fiore et al ).…”

Section: Discussionmentioning

confidence: 99%

Abiotic conditions drive significant variability in nutrient processing by a common Caribbean sponge, Ircinia felix

Archer

Stevens

Rossi

et al. 2017

Limnology & Oceanography

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Coral reefs typically occur in oligotrophic waters, where tight recycling of energy and nutrients is essential in order to support their high productivity. Sponges are efficient filter feeders that host diverse and abundant microbial communities that often contain members capable of carrying out complex nutrient transformations. Consequently, sponges often act as significant sources of bioavailable forms of nitrogen and phosphorus while acting as sinks for dissolved organic carbon (DOC). However, little attention has focused on variability of nutrient release by sponges and no studies have reported how abiotic conditions may impact sponge‐driven changes in nutrient concentrations. Here, we show that a common Caribbean sponge, Ircinia felix, is capable of being both a source and a sink for DOC, ammonium, nitrate/nitrite ( NOx−), and phosphate ( PO43−). Additionally, we show that abiotic conditions, particularly ambient nutrient availability, seem to explain a significant amount of the variability (R2 range from 0.40 to 0.65). Interestingly, as ambient nutrient concentrations increased, I. felix transitioned from acting as a source to serving as a sink for all nutrient forms measured. We also found I. felix‐associated bacteria exhibit a significantly higher abundance of predicted nitrogen metabolism, carbon fixation, and photosynthetic genes relative to ambient water and sediment. These results suggest that sponges play an important and dynamic role in biogeochemical cycling on reefs, particularly as human activities alter natural nutrient dynamics in coastal systems.

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Section: Discussionmentioning

confidence: 99%

Abiotic conditions drive significant variability in nutrient processing by a common Caribbean sponge, Ircinia felix

Archer

Stevens

Rossi

et al. 2017

Limnology & Oceanography

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“…While many sponge species host highly stable microbiomes irrespective of environment37383940, recent research has also indicated that shifts in the sponge-associated microbial community may confer a mechanism for local host acclimation to different environmental conditions41. The large shifts in the microbiome of C. foliascens and C. orientalis under low light conditions, including the appearance of novel photosynthetic microorganisms under highly light attenuated conditions (DLI of 0.8 mol photons m −2 d −1 ), may indicate an attempt at symbiont shuffling to a community better able to function under reduced irradiance.…”

Section: Discussionmentioning

confidence: 99%

Effects of light attenuation on the sponge holobiont- implications for dredging management

Pineda

Strehlow

Duckworth

et al. 2016

Sci Rep

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Dredging and natural sediment resuspension events can cause high levels of turbidity, reducing the amount of light available for photosynthetic benthic biota. To determine how marine sponges respond to light attenuation, five species were experimentally exposed to a range of light treatments. Tolerance thresholds and capacity for recovery varied markedly amongst species. Whilst light attenuation had no effect on the heterotrophic species Stylissa flabelliformis and Ianthella basta, the phototrophic species Cliona orientalis and Carteriospongia foliascens discoloured (bleached) over a 28 day exposure period to very low light (<0.8 mol photons m−2 d−1). In darkness, both species discoloured within a few days, concomitant with reduced fluorescence yields, chlorophyll concentrations and shifts in their associated microbiomes. The phototrophic species Cymbastela coralliophila was less impacted by light reduction. C. orientalis and C. coralliophila exhibited full recovery under normal light conditions, whilst C. foliascens did not recover and showed high levels of mortality. The light treatments used in the study are directly relevant to conditions that can occur in situ during dredging projects, indicating that light attenuation poses a risk to photosynthetic marine sponges. Examining benthic light levels over temporal scales would enable dredging proponents to be aware of conditions that could impact on sponge physiology.

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“…Similar resistance has been seen in other host-symbiont systems. For example, when exposed to thermal, nutrient, and food shortage stressors, no clear changes in sponge symbiont communities have been observed, even though these stressors can lead to host death in some instances (47,48).…”

Section: Discussionmentioning

confidence: 99%

Short-Term Exposure to Coal Combustion Waste Has Little Impact on the Skin Microbiome of Adult Spring Peepers (Pseudacris crucifer)

Hughey

Walke

Becker

et al. 2016

Appl Environ Microbiol

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Disruptions to the microbiome can impact host health as can exposure to environmental contaminants. However, few studies have addressed how environmental contaminants impact the microbiome. We explored this question for frogs that breed in wetlands contaminated with fly ash, a by-product of coal combustion that is enriched in trace elements. We found differences in the bacterial communities among a fly ash-contaminated site and several reference wetlands. We then experimentally assessed the impacts of fly ash on the skin microbiome of adult spring peepers (Pseudacris crucifer). Frogs were exposed to fly ash in the laboratory for 12 h, the duration of a typical breeding event, and the skin microbiome was assessed after 5 days (experiment 1) or after 5 and 15 days (experiment 2). We examined bacterial community structure using 16S rRNA gene amplicon sequencing and metabolite profiles using high-pressure liquid chromatography-mass spectrometry (HPLC-MS). We found little impact as the result of acute exposure to fly ash on the bacterial communities or metabolite profiles in either experiment, suggesting that the bacterial symbiont communities of adults may be relatively resistant to brief contaminant exposure. However, housing frogs in the laboratory altered bacterial community structure in the two experiments, which supports prior research suggesting that environmental source pools are important for maintaining the amphibian skin microbiome. Therefore, for contaminants like fly ash that may alter the potential source pool of symbionts, we think it may be important to explore how contaminants affect the initial assembly of the amphibian skin microbiome in larval amphibians that develop within contaminated sites. IMPORTANCEAnimals are hosts to many symbiotic microorganisms, collectively called the microbiome, that play critical roles in host health. Therefore, environmental contaminants that alter the microbiome may impact hosts. Some of the most widespread contaminants, produced worldwide, are derived from the mining, storage, and combustion of coal for energy. Fly ash, for example, is a by-product of coal combustion. It contains compounds such as arsenic, selenium, cadmium, and strontium and is a recognized source of ground and surface water contamination. Here, we experimentally investigated the impacts of short-term fly ash exposure on the skin microbiome of spring peepers, one of many species of amphibian that sometimes breed in open fly ash disposal ponds. This research provides a look into the potential impacts of fly ash on an animal's microbiome and suggests important future directions for research on the effects of environmental contaminants on the microbiome. Vertebrates host a wide array of symbiotic microorganisms, mainly in the gut, but there are unique microbial communities spread throughout the body from the nasal cavity to the lungs to the skin (1). While we have long understood that the microbiota residing in the gut are diverse and are important in helping to digest food, only recently have...

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Sponge-Microbe Associations Survive High Nutrients and Temperatures

Cited by 74 publications

References 115 publications

Abiotic conditions drive significant variability in nutrient processing by a common Caribbean sponge, Ircinia felix

Abiotic conditions drive significant variability in nutrient processing by a common Caribbean sponge, Ircinia felix

Effects of light attenuation on the sponge holobiont- implications for dredging management

Short-Term Exposure to Coal Combustion Waste Has Little Impact on the Skin Microbiome of Adult Spring Peepers (Pseudacris crucifer)

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