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

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 e...

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Main Authors: Huilong Ou, Mingyu Li, Shufei Wu, Linli Jia, Russell T. Hill, Jing Zhao
Format: Article
Language:English
Published: MDPI AG 2019-12-01
Series:Microorganisms
Subjects:
Online Access:https://www.mdpi.com/2076-2607/8/1/63
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spelling doaj-d57e6061709344168cb32e3c20cc3c882020-11-25T02:56:45ZengMDPI AGMicroorganisms2076-26072019-12-01816310.3390/microorganisms8010063microorganisms8010063Characteristic Microbiomes Correlate with Polyphosphate Accumulation of Marine Sponges in South China Sea AreasHuilong Ou0Mingyu Li1Shufei Wu2Linli Jia3Russell T. Hill4Jing Zhao5College of Ocean and Earth Science of Xiamen University, Xiamen 361005, ChinaCollege of Ocean and Earth Science of Xiamen University, Xiamen 361005, ChinaCollege of Ocean and Earth Science of Xiamen University, Xiamen 361005, ChinaCollege of Ocean and Earth Science of Xiamen University, Xiamen 361005, ChinaInstitute of Marine and Environmental Technology, University of Maryland Center for Environmental Science, Baltimore, MD 21202, USACollege of Ocean and Earth Science of Xiamen University, Xiamen 361005, ChinaSome 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., <i>Mycale</i> sp. or <i>Callyspongia</i> 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 (<i>ppk</i>) 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 <i>Synechococcus</i>, <i>Rhodopirellula</i>, <i>Blastopirellula,</i> and <i>Rubripirellula</i>. About 50% of <i>ppk</i> genes obtained from the total DNA of sponge holobionts, had above 80% amino acid sequence similarities to those sequences from <i>Synechococcus</i>. In general, it suggested that sponges employed differentiated strategies towards the use of phosphorus in different nutrient environments and the symbiotic <i>Synechococcus</i> could play a key role in accumulating polyP.https://www.mdpi.com/2076-2607/8/1/63spongepolyphosphatemicrobiomes<i>ppk</i> gene
collection DOAJ
language English
format Article
sources DOAJ
author Huilong Ou
Mingyu Li
Shufei Wu
Linli Jia
Russell T. Hill
Jing Zhao
spellingShingle Huilong Ou
Mingyu Li
Shufei Wu
Linli Jia
Russell T. Hill
Jing Zhao
Characteristic Microbiomes Correlate with Polyphosphate Accumulation of Marine Sponges in South China Sea Areas
Microorganisms
sponge
polyphosphate
microbiomes
<i>ppk</i> gene
author_facet Huilong Ou
Mingyu Li
Shufei Wu
Linli Jia
Russell T. Hill
Jing Zhao
author_sort Huilong Ou
title Characteristic Microbiomes Correlate with Polyphosphate Accumulation of Marine Sponges in South China Sea Areas
title_short Characteristic Microbiomes Correlate with Polyphosphate Accumulation of Marine Sponges in South China Sea Areas
title_full Characteristic Microbiomes Correlate with Polyphosphate Accumulation of Marine Sponges in South China Sea Areas
title_fullStr Characteristic Microbiomes Correlate with Polyphosphate Accumulation of Marine Sponges in South China Sea Areas
title_full_unstemmed Characteristic Microbiomes Correlate with Polyphosphate Accumulation of Marine Sponges in South China Sea Areas
title_sort characteristic microbiomes correlate with polyphosphate accumulation of marine sponges in south china sea areas
publisher MDPI AG
series Microorganisms
issn 2076-2607
publishDate 2019-12-01
description 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., <i>Mycale</i> sp. or <i>Callyspongia</i> 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 (<i>ppk</i>) 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 <i>Synechococcus</i>, <i>Rhodopirellula</i>, <i>Blastopirellula,</i> and <i>Rubripirellula</i>. About 50% of <i>ppk</i> genes obtained from the total DNA of sponge holobionts, had above 80% amino acid sequence similarities to those sequences from <i>Synechococcus</i>. In general, it suggested that sponges employed differentiated strategies towards the use of phosphorus in different nutrient environments and the symbiotic <i>Synechococcus</i> could play a key role in accumulating polyP.
topic sponge
polyphosphate
microbiomes
<i>ppk</i> gene
url https://www.mdpi.com/2076-2607/8/1/63
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