Characteristic Microbiomes Correlate with Polyphosphate Accumulation of Marine Sponges in South China Sea Areas.

Huilong Ou,Russell T Hill,Shufei Wu,Mingyu Li,Jing Zhao,Linli Jia

doi:10.3390/microorganisms8010063

Abstract

Some sponges have been shown to accumulate abundant phosphorus in the form of polyphosphate (polyP) granules even in waters where phosphorus is present at low concentrations. But the polyP accumulation occurring in sponges and their symbiotic bacteria have been little studied. The amounts of polyP exhibited significant differences in twelve sponges from marine environments with high or low dissolved inorganic phosphorus (DIP) concentrations which were quantified by spectral analysis, even though in the same sponge genus, e.g., Mycale sp. or Callyspongia sp. PolyP enrichment rates of sponges in oligotrophic environments were far higher than those in eutrophic environments. Massive polyP granules were observed under confocal microscopy in samples from very low DIP environments. The composition of sponge symbiotic microbes was analyzed by high-throughput sequencing and the corresponding polyphosphate kinase (ppk) genes were detected. Sequence analysis revealed that in the low DIP environment, those sponges with higher polyP content and enrichment rates had relatively higher abundances of cyanobacteria. Mantel tests and canonical correspondence analysis (CCA) examined that the polyP enrichment rate was most strongly correlated with the structure of microbial communities, including genera Synechococcus, Rhodopirellula, Blastopirellula, and Rubripirellula. About 50% of ppk genes obtained from the total DNA of sponge holobionts, had above 80% amino acid sequence similarities to those sequences from Synechococcus. In general, it suggested that sponges employed differentiated strategies towards the use of phosphorus in different nutrient environments and the symbiotic Synechococcus could play a key role in accumulating polyP.

Highlights

Marine sponges are ubiquitous in marine environments and can filter large amounts of water and mediate nutrient transformations by virtue of respiring organic matter and facilitating the consumption and release of nutrients [1,2]
Sampling sites in the South China Sea were divided into high dissolved inorganic phosphorus (DIP) and low DIP areas based on the value in water samples and location (Table 1)
The amounts of polyP accumulated by sponge in Dongshan Bay were significantly different, with 0.024 ± 0.001 mg/g detected in Callyspongia sp. (DC), and 0.008 ± 0.004 mg/g detected in Mycale sp. (DM) which was the lowest in all samples detected, while as much as 3.722 ± 0.152 mg/g was detected in Tedania sp. (DT)

Summary

Introduction

Marine sponges are ubiquitous in marine environments and can filter large amounts of water and mediate nutrient transformations by virtue of respiring organic matter and facilitating the consumption and release of nutrients [1,2]. Zhang et al [14] discovered a major role for sponges with regard to the marine phosphorus cycle, in which phosphorus is sequestrated in the form of polyphosphate by the microbial symbionts of marine sponges. The ability of bacterial symbionts in sponges to concentrate phosphorus and store it in the form of polyphosphate raises the possibility that sponges may play a role as a sink of phosphorus and keep themselves thriving under the extremely low nutrient conditions in the marine reef ecosystems. Polyphosphate (polyP) production and storage by sponge endosymbionts, the P distribution in other sponge reef ecosystems, those in extremely low nutrient environments, and the specific symbiotic microbial community response to polyphosphate sequestration have rarely been studied

Objectives

Methods

Results

Conclusion