A novel Chromatiales bacterium is a potential sulfide oxidizer in multiple orders of marine sponges

Lavy, Adi; Keren, Ray; Yu, Ke; Thomas, Brian C.; Alvarez‐Cohen, Lisa; Banfield, Jillian F.; Ilan, Micha

doi:10.1111/1462-2920.14013

Cited by 28 publications

(12 citation statements)

References 96 publications

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“…7 ). Chemoautotrophic members of the sponge microbiome can utilise inorganic C produced during host respiration [ 70 , 75 , 76 ] and microbial N metabolism can be driven by the assimilation or remineralisation of sponge-excreted nitrogenous wastes [ 20 , 71 – 73 , 77 ]. Indeed, ammonia-oxidising archaea and bacteria have been detected in H. caerulea [ 74 ].…”

Section: Discussionmentioning

confidence: 99%

Subcellular view of host–microbiome nutrient exchange in sponges: insights into the ecological success of an early metazoan–microbe symbiosis

et al. 2021

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Background Sponges are increasingly recognised as key ecosystem engineers in many aquatic habitats. They play an important role in nutrient cycling due to their unrivalled capacity for processing both dissolved and particulate organic matter (DOM and POM) and the exceptional metabolic repertoire of their diverse and abundant microbial communities. Functional studies determining the role of host and microbiome in organic nutrient uptake and exchange, however, are limited. Therefore, we coupled pulse-chase isotopic tracer techniques with nanoscale secondary ion mass spectrometry (NanoSIMS) to visualise the uptake and translocation of 13C- and 15N-labelled dissolved and particulate organic food at subcellular level in the high microbial abundance sponge Plakortis angulospiculatus and the low microbial abundance sponge Halisarca caerulea. Results The two sponge species showed significant enrichment of DOM- and POM-derived 13C and 15N into their tissue over time. Microbial symbionts were actively involved in the assimilation of DOM, but host filtering cells (choanocytes) appeared to be the primary site of DOM and POM uptake in both sponge species overall, via pinocytosis and phagocytosis, respectively. Translocation of carbon and nitrogen from choanocytes to microbial symbionts occurred over time, irrespective of microbial abundance, reflecting recycling of host waste products by the microbiome. Conclusions Here, we provide empirical evidence indicating that the prokaryotic communities of a high and a low microbial abundance sponge obtain nutritional benefits from their host-associated lifestyle. The metabolic interaction between the highly efficient filter-feeding host and its microbial symbionts likely provides a competitive advantage to the sponge holobiont in the oligotrophic environments in which they thrive, by retaining and recycling limiting nutrients. Sponges present a unique model to link nutritional symbiotic interactions to holobiont function, and, via cascading effects, ecosystem functioning, in one of the earliest metazoan–microbe symbioses.

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Section: Discussionmentioning

confidence: 99%

Subcellular view of host–microbiome nutrient exchange in sponges: insights into the ecological success of an early metazoan–microbe symbiosis

et al. 2021

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“…To note, the highest increase in relative abundance after treatment was noticed for the Chromatiales for which their contribution increased from 0.82 to 6.83%. The Chromatiales belong to the γ- proteobacteria containing a variety of electrogenic bacteria 39 . In addition, Pseudomonadales which can secret redox mediators were found in YN2, indicating it can provide electron transfer mediators to other microorganisms while improving its own power generation capacity 40 .…”

Section: Resultsmentioning

confidence: 99%

The oil removal and the characteristics of changes in the composition of bacteria based on the oily sludge bioelectrochemical system

Guo

Tang

Wang

et al. 2020

Sci Rep

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Microbial fuel cell (MFC) technology is a simple way to accelerate the treatment of the oily sludge which is a major problem affecting the quality of oil fields and surrounding environment while generating electricity. To investigate the oil removal and the characteristics of changes in the composition of bacteria, sediment microbial fuel cells (SMFCs) supplemented with oily sludge was constructed. The results showed that the degradation efficiency of total petroleum hydrocarbon (TPH) of SMFC treatment was 10.1 times higher than the common anaerobic degradation. In addition, the degradation rate of n-alkanes followed the order of high carbon number > low carbon number > medium carbon number. The odd–even alkane predominance (OEP) increased, indicating that a high contribution of even alkanes whose degradation predominates. The OUT number, Shannon index, AEC index, and Chao1 index of the sludge treated with SMFC (YN2) are greater than those of the original sludge (YN1), showing that the microbial diversity of sludge increased after SMFC treatment. After SMFC treatment the relative abundance of Chloroflexi, Bacteroidia and Pseudomonadales which are essential for the degradation of the organic matter and electricity production increased significantly in YN2. These results will play a crucial role in improving the performance of oily sludge MFC.

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“…Sulfur metabolism, whether through oxidation and reduction of sulfur compounds for energy and the subsequent fixation of carbon or through assimilation of organic sulfur compounds (e.g., APS, DMSP), appears to be prevalent in sponge-microbe systems (Hoffmann et al, 2005a,b;Fiore et al, 2015a;Jensen et al, 2017;Lavy et al, 2018;Podell et al, 2019;Zhang et al, 2019;Engelberts et al, 2020). Sulfur-based symbioses have been documented in other invertebrates (e.g., Cavanaugh et al, 1981;Southward et al, 1981;Fisher and Childress, 1984;Dubilier et al, 2001) and have potential to be a common trait in marine invertebrate systems (Fiore et al, 2020).…”

Section: Diversity Of Resources and Symbiont Metabolismmentioning

confidence: 99%

Sponge–Microbe Interactions on Coral Reefs: Multiple Evolutionary Solutions to a Complex Environment

et al. 2021

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Marine sponges have been successful in their expansion across diverse ecological niches around the globe. Pioneering work attributed this success to both a well-developed aquiferous system that allowed for efficient filter feeding on suspended organic matter and the presence of microbial symbionts that can supplement host heterotrophic feeding with photosynthate or dissolved organic carbon. We now know that sponge-microbe interactions are host-specific, highly nuanced, and provide diverse nutritional benefits to the host sponge. Despite these advances in the field, many current hypotheses pertaining to the evolution of these interactions are overly generalized; these over-simplifications limit our understanding of the evolutionary processes shaping these symbioses and how they contribute to the ecological success of sponges on modern coral reefs. To highlight the current state of knowledge in this field, we start with seminal papers and review how contemporary work using higher resolution techniques has both complemented and challenged their early hypotheses. We outline different schools of thought by discussing evidence of symbiont contribution to both host ecological divergence and convergence, nutritional specificity and plasticity, and allopatric and sympatric speciation. Based on this synthesis, we conclude that the evolutionary pressures shaping these interactions are complex, with influences from both external (nutrient limitation and competition) and internal (fitness trade-offs and evolutionary constraints) factors. We outline recent controversies pertaining to these evolutionary pressures and place our current understanding of these interactions into a broader ecological and evolutionary framework. Finally, we propose areas for future research that we believe will lead to important new developments in the field.

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A novel Chromatiales bacterium is a potential sulfide oxidizer in multiple orders of marine sponges

Cited by 28 publications

References 96 publications

Subcellular view of host–microbiome nutrient exchange in sponges: insights into the ecological success of an early metazoan–microbe symbiosis

Subcellular view of host–microbiome nutrient exchange in sponges: insights into the ecological success of an early metazoan–microbe symbiosis

The oil removal and the characteristics of changes in the composition of bacteria based on the oily sludge bioelectrochemical system

Sponge–Microbe Interactions on Coral Reefs: Multiple Evolutionary Solutions to a Complex Environment

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