An alternative polysaccharide uptake mechanism of marine bacteria

Greta Reintjes, Carol Arnosti, Bernhard M. Fuchs, Rudolf Amann

Research output: Contribution to journalArticle

  • 7 Citations

Abstract

Heterotrophic microbial communities process much of the carbon fixed by phytoplankton in the ocean, thus having a critical role in the global carbon cycle. A major fraction of the phytoplankton-derived substrates are high-molecular-weight (HMW) polysaccharides. For bacterial uptake, these substrates must initially be hydrolysed to smaller sizes by extracellular enzymes. We investigated polysaccharide hydrolysis by microbial communities during a transect of the Atlantic Ocean, and serendipitously discovered - using super-resolution structured illumination microscopy - that up to 26% of total cells showed uptake of fluorescently labelled polysaccharides (FLA-PS). Fluorescence in situ hybridisation identified these organisms as members of the bacterial phyla Bacteroidetes and Planctomycetes and the gammaproteobacterial genus Catenovulum. Simultaneous membrane staining with nile red indicated that the FLA-PS labelling occurred in the cell but not in the cytoplasm. The dynamics of FLA-PS staining was further investigated in pure culture experiments using Gramella forsetii, a marine member of Bacteroidetes. The staining patterns observed in environmental samples and pure culture tests are consistent with a 'selfish' uptake mechanisms of larger oligosaccharides (>600 Da), as demonstrated for gut Bacteroidetes. Ecologically, this alternative polysaccharide uptake mechanism secures substantial quantities of substrate in the periplasmic space, where further processing can occur without diffusive loss. Such a mechanism challenges the paradigm that hydrolysis of HMW substrates inevitably yields low-molecular-weight fragments that are available to the surrounding community and demonstrates the importance of an alternative mechanism of polysaccharide uptake in marine bacteria.

LanguageEnglish (US)
Pages1640-1650
Number of pages11
JournalISME Journal
Volume11
Issue number7
DOIs
StatePublished - Jul 1 2017

Fingerprint

polysaccharide
Polysaccharides
polysaccharides
Bacteria
uptake mechanisms
bacterium
Bacteroidetes
bacteria
Phytoplankton
substrate
Molecular Weight
Staining and Labeling
molecular weight
microbial communities
microbial community
hydrolysis
Hydrolysis
phytoplankton
Atlantic Ocean
Carbon Cycle

ASJC Scopus subject areas

  • Microbiology
  • Ecology, Evolution, Behavior and Systematics

Cite this

Reintjes, G., Arnosti, C., Fuchs, B. M., & Amann, R. (2017). An alternative polysaccharide uptake mechanism of marine bacteria. ISME Journal, 11(7), 1640-1650. DOI: 10.1038/ismej.2017.26

An alternative polysaccharide uptake mechanism of marine bacteria. / Reintjes, Greta; Arnosti, Carol; Fuchs, Bernhard M.; Amann, Rudolf.

In: ISME Journal, Vol. 11, No. 7, 01.07.2017, p. 1640-1650.

Research output: Contribution to journalArticle

Reintjes, G, Arnosti, C, Fuchs, BM & Amann, R 2017, 'An alternative polysaccharide uptake mechanism of marine bacteria' ISME Journal, vol 11, no. 7, pp. 1640-1650. DOI: 10.1038/ismej.2017.26
Reintjes G, Arnosti C, Fuchs BM, Amann R. An alternative polysaccharide uptake mechanism of marine bacteria. ISME Journal. 2017 Jul 1;11(7):1640-1650. Available from, DOI: 10.1038/ismej.2017.26
Reintjes, Greta ; Arnosti, Carol ; Fuchs, Bernhard M. ; Amann, Rudolf. / An alternative polysaccharide uptake mechanism of marine bacteria. In: ISME Journal. 2017 ; Vol. 11, No. 7. pp. 1640-1650
@article{f529a18015734ea4aeae7eba2e3e5e6a,
title = "An alternative polysaccharide uptake mechanism of marine bacteria",
abstract = "Heterotrophic microbial communities process much of the carbon fixed by phytoplankton in the ocean, thus having a critical role in the global carbon cycle. A major fraction of the phytoplankton-derived substrates are high-molecular-weight (HMW) polysaccharides. For bacterial uptake, these substrates must initially be hydrolysed to smaller sizes by extracellular enzymes. We investigated polysaccharide hydrolysis by microbial communities during a transect of the Atlantic Ocean, and serendipitously discovered - using super-resolution structured illumination microscopy - that up to 26{\%} of total cells showed uptake of fluorescently labelled polysaccharides (FLA-PS). Fluorescence in situ hybridisation identified these organisms as members of the bacterial phyla Bacteroidetes and Planctomycetes and the gammaproteobacterial genus Catenovulum. Simultaneous membrane staining with nile red indicated that the FLA-PS labelling occurred in the cell but not in the cytoplasm. The dynamics of FLA-PS staining was further investigated in pure culture experiments using Gramella forsetii, a marine member of Bacteroidetes. The staining patterns observed in environmental samples and pure culture tests are consistent with a 'selfish' uptake mechanisms of larger oligosaccharides (>600 Da), as demonstrated for gut Bacteroidetes. Ecologically, this alternative polysaccharide uptake mechanism secures substantial quantities of substrate in the periplasmic space, where further processing can occur without diffusive loss. Such a mechanism challenges the paradigm that hydrolysis of HMW substrates inevitably yields low-molecular-weight fragments that are available to the surrounding community and demonstrates the importance of an alternative mechanism of polysaccharide uptake in marine bacteria.",
author = "Greta Reintjes and Carol Arnosti and Fuchs, {Bernhard M.} and Rudolf Amann",
year = "2017",
month = "7",
day = "1",
doi = "10.1038/ismej.2017.26",
language = "English (US)",
volume = "11",
pages = "1640--1650",
journal = "ISME Journal",
issn = "1751-7362",
publisher = "Nature Publishing Group",
number = "7",

}

TY - JOUR

T1 - An alternative polysaccharide uptake mechanism of marine bacteria

AU - Reintjes,Greta

AU - Arnosti,Carol

AU - Fuchs,Bernhard M.

AU - Amann,Rudolf

PY - 2017/7/1

Y1 - 2017/7/1

N2 - Heterotrophic microbial communities process much of the carbon fixed by phytoplankton in the ocean, thus having a critical role in the global carbon cycle. A major fraction of the phytoplankton-derived substrates are high-molecular-weight (HMW) polysaccharides. For bacterial uptake, these substrates must initially be hydrolysed to smaller sizes by extracellular enzymes. We investigated polysaccharide hydrolysis by microbial communities during a transect of the Atlantic Ocean, and serendipitously discovered - using super-resolution structured illumination microscopy - that up to 26% of total cells showed uptake of fluorescently labelled polysaccharides (FLA-PS). Fluorescence in situ hybridisation identified these organisms as members of the bacterial phyla Bacteroidetes and Planctomycetes and the gammaproteobacterial genus Catenovulum. Simultaneous membrane staining with nile red indicated that the FLA-PS labelling occurred in the cell but not in the cytoplasm. The dynamics of FLA-PS staining was further investigated in pure culture experiments using Gramella forsetii, a marine member of Bacteroidetes. The staining patterns observed in environmental samples and pure culture tests are consistent with a 'selfish' uptake mechanisms of larger oligosaccharides (>600 Da), as demonstrated for gut Bacteroidetes. Ecologically, this alternative polysaccharide uptake mechanism secures substantial quantities of substrate in the periplasmic space, where further processing can occur without diffusive loss. Such a mechanism challenges the paradigm that hydrolysis of HMW substrates inevitably yields low-molecular-weight fragments that are available to the surrounding community and demonstrates the importance of an alternative mechanism of polysaccharide uptake in marine bacteria.

AB - Heterotrophic microbial communities process much of the carbon fixed by phytoplankton in the ocean, thus having a critical role in the global carbon cycle. A major fraction of the phytoplankton-derived substrates are high-molecular-weight (HMW) polysaccharides. For bacterial uptake, these substrates must initially be hydrolysed to smaller sizes by extracellular enzymes. We investigated polysaccharide hydrolysis by microbial communities during a transect of the Atlantic Ocean, and serendipitously discovered - using super-resolution structured illumination microscopy - that up to 26% of total cells showed uptake of fluorescently labelled polysaccharides (FLA-PS). Fluorescence in situ hybridisation identified these organisms as members of the bacterial phyla Bacteroidetes and Planctomycetes and the gammaproteobacterial genus Catenovulum. Simultaneous membrane staining with nile red indicated that the FLA-PS labelling occurred in the cell but not in the cytoplasm. The dynamics of FLA-PS staining was further investigated in pure culture experiments using Gramella forsetii, a marine member of Bacteroidetes. The staining patterns observed in environmental samples and pure culture tests are consistent with a 'selfish' uptake mechanisms of larger oligosaccharides (>600 Da), as demonstrated for gut Bacteroidetes. Ecologically, this alternative polysaccharide uptake mechanism secures substantial quantities of substrate in the periplasmic space, where further processing can occur without diffusive loss. Such a mechanism challenges the paradigm that hydrolysis of HMW substrates inevitably yields low-molecular-weight fragments that are available to the surrounding community and demonstrates the importance of an alternative mechanism of polysaccharide uptake in marine bacteria.

UR - http://www.scopus.com/inward/record.url?scp=85015758927&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85015758927&partnerID=8YFLogxK

U2 - 10.1038/ismej.2017.26

DO - 10.1038/ismej.2017.26

M3 - Article

VL - 11

SP - 1640

EP - 1650

JO - ISME Journal

T2 - ISME Journal

JF - ISME Journal

SN - 1751-7362

IS - 7

ER -