PMID- 31728021
OWN - NLM
STAT- MEDLINE
DCOM- 20200422
LR  - 20220417
IS  - 1751-7370 (Electronic)
IS  - 1751-7362 (Print)
IS  - 1751-7362 (Linking)
VI  - 14
IP  - 2
DP  - 2020 Feb
TI  - Groundwater cable bacteria conserve energy by sulfur disproportionation.
PG  - 623-634
LID - 10.1038/s41396-019-0554-1 [doi]
AB  - Cable bacteria of the family Desulfobulbaceae couple spatially separated sulfur 
      oxidation and oxygen or nitrate reduction by long-distance electron transfer, 
      which can constitute the dominant sulfur oxidation process in shallow sediments. 
      However, it remains unknown how cells in the anoxic part of the centimeter-long 
      filaments conserve energy. We found 16S rRNA gene sequences similar to 
      groundwater cable bacteria in a 1-methylnaphthalene-degrading culture (1MN). 
      Cultivation with elemental sulfur and thiosulfate with ferrihydrite or nitrate as 
      electron acceptors resulted in a first cable bacteria enrichment culture 
      dominated >90% by 16S rRNA sequences belonging to the Desulfobulbaceae. 
      Desulfobulbaceae-specific fluorescence in situ hybridization (FISH) unveiled 
      single cells and filaments of up to several hundred micrometers length to belong 
      to the same species. The Desulfobulbaceae filaments also showed the distinctive 
      cable bacteria morphology with their continuous ridge pattern as revealed by 
      atomic force microscopy. The cable bacteria grew with nitrate as electron 
      acceptor and elemental sulfur and thiosulfate as electron donor, but also by 
      sulfur disproportionation when Fe(Cl)(2) or Fe(OH)(3) were present as sulfide 
      scavengers. Metabolic reconstruction based on the first nearly complete genome of 
      groundwater cable bacteria revealed the potential for sulfur disproportionation 
      and a chemo-litho-autotrophic metabolism. The presence of different types of 
      hydrogenases in the genome suggests that they can utilize hydrogen as alternative 
      electron donor. Our results imply that cable bacteria not only use sulfide 
      oxidation coupled to oxygen or nitrate reduction by LDET for energy conservation, 
      but sulfur disproportionation might constitute the energy metabolism for cells in 
      large parts of the cable bacterial filaments.
FAU - Muller, Hubert
AU  - Muller H
AD  - Biofilm Center, University of Duisburg-Essen, Universitatsstr. 5, 45141, Essen, 
      Germany.
FAU - Marozava, Sviatlana
AU  - Marozava S
AD  - Institute of Groundwater Ecology, Helmholtz Zentrum Munchen, Ingolstadter 
      Landstrasse 1, 85764, Neuherberg, Germany.
FAU - Probst, Alexander J
AU  - Probst AJ
AD  - Biofilm Center, University of Duisburg-Essen, Universitatsstr. 5, 45141, Essen, 
      Germany.
FAU - Meckenstock, Rainer U
AU  - Meckenstock RU
AD  - Biofilm Center, University of Duisburg-Essen, Universitatsstr. 5, 45141, Essen, 
      Germany. rainer.meckenstock@uni-due.de.
LA  - eng
GR  - 666952/ERC_/European Research Council/International
PT  - Journal Article
PT  - Research Support, Non-U.S. Gov't
DEP - 20191114
PL  - England
TA  - ISME J
JT  - The ISME journal
JID - 101301086
RN  - 0 (Nitrates)
RN  - 0 (RNA, Ribosomal, 16S)
RN  - 0 (Sulfides)
RN  - 70FD1KFU70 (Sulfur)
SB  - IM
MH  - *Deltaproteobacteria/classification/genetics/metabolism
MH  - *Energy Metabolism
MH  - Environmental Microbiology
MH  - Groundwater/*microbiology
MH  - In Situ Hybridization, Fluorescence
MH  - Microscopy, Atomic Force
MH  - Nitrates/metabolism
MH  - Phylogeny
MH  - RNA, Ribosomal, 16S/genetics
MH  - Sulfides/metabolism
MH  - Sulfur/metabolism
MH  - Water Microbiology
PMC - PMC6976610
MID - EMS84818
COIS- The authors declare that they have no conflict of interest.
EDAT- 2019/11/16 06:00
MHDA- 2020/04/23 06:00
PMCR- 2019/11/14
CRDT- 2019/11/16 06:00
PHST- 2019/07/03 00:00 [received]
PHST- 2019/11/04 00:00 [accepted]
PHST- 2019/10/28 00:00 [revised]
PHST- 2019/11/16 06:00 [pubmed]
PHST- 2020/04/23 06:00 [medline]
PHST- 2019/11/16 06:00 [entrez]
PHST- 2019/11/14 00:00 [pmc-release]
AID - 10.1038/s41396-019-0554-1 [pii]
AID - 554 [pii]
AID - 10.1038/s41396-019-0554-1 [doi]
PST - ppublish
SO  - ISME J. 2020 Feb;14(2):623-634. doi: 10.1038/s41396-019-0554-1. Epub 2019 Nov 14.