Proliferation of hydrocarbon-degrading microbes at the bottom of the Mariana Trench.


Journal

Microbiome
ISSN: 2049-2618
Titre abrégé: Microbiome
Pays: England
ID NLM: 101615147

Informations de publication

Date de publication:
12 04 2019
Historique:
received: 25 11 2018
accepted: 22 02 2019
entrez: 13 4 2019
pubmed: 13 4 2019
medline: 21 6 2019
Statut: epublish

Résumé

The Mariana Trench is the deepest known site in the Earth's oceans, reaching a depth of ~ 11,000 m at the Challenger Deep. Recent studies reveal that hadal waters harbor distinctive microbial planktonic communities. However, the genetic potential of microbial communities within the hadal zone is poorly understood. Here, implementing both culture-dependent and culture-independent methods, we perform extensive analysis of microbial populations and their genetic potential at different depths in the Mariana Trench. Unexpectedly, we observed an abrupt increase in the abundance of hydrocarbon-degrading bacteria at depths > 10,400 m in the Challenger Deep. Indeed, the proportion of hydrocarbon-degrading bacteria at > 10,400 m is the highest observed in any natural environment on Earth. These bacteria were mainly Oleibacter, Thalassolituus, and Alcanivorax genera, all of which include species known to consume aliphatic hydrocarbons. This community shift towards hydrocarbon degraders was accompanied by increased abundance and transcription of genes involved in alkane degradation. Correspondingly, three Alcanivorax species that were isolated from 10,400 m water supplemented with hexadecane were able to efficiently degrade n-alkanes under conditions simulating the deep sea, as did a reference Oleibacter strain cultured at atmospheric pressure. Abundant n-alkanes were observed in sinking particles at 2000, 4000, and 6000 m (averaged 23.5 μg/gdw) and hadal surface sediments at depths of 10,908, 10,909, and 10,911 m (averaged 2.3 μg/gdw). The δ These results reveal that hydrocarbon-degrading microorganisms are present in great abundance in the deepest seawater on Earth and shed a new light on potential biological processes in this extreme environment.

Sections du résumé

BACKGROUND
The Mariana Trench is the deepest known site in the Earth's oceans, reaching a depth of ~ 11,000 m at the Challenger Deep. Recent studies reveal that hadal waters harbor distinctive microbial planktonic communities. However, the genetic potential of microbial communities within the hadal zone is poorly understood.
RESULTS
Here, implementing both culture-dependent and culture-independent methods, we perform extensive analysis of microbial populations and their genetic potential at different depths in the Mariana Trench. Unexpectedly, we observed an abrupt increase in the abundance of hydrocarbon-degrading bacteria at depths > 10,400 m in the Challenger Deep. Indeed, the proportion of hydrocarbon-degrading bacteria at > 10,400 m is the highest observed in any natural environment on Earth. These bacteria were mainly Oleibacter, Thalassolituus, and Alcanivorax genera, all of which include species known to consume aliphatic hydrocarbons. This community shift towards hydrocarbon degraders was accompanied by increased abundance and transcription of genes involved in alkane degradation. Correspondingly, three Alcanivorax species that were isolated from 10,400 m water supplemented with hexadecane were able to efficiently degrade n-alkanes under conditions simulating the deep sea, as did a reference Oleibacter strain cultured at atmospheric pressure. Abundant n-alkanes were observed in sinking particles at 2000, 4000, and 6000 m (averaged 23.5 μg/gdw) and hadal surface sediments at depths of 10,908, 10,909, and 10,911 m (averaged 2.3 μg/gdw). The δ
CONCLUSIONS
These results reveal that hydrocarbon-degrading microorganisms are present in great abundance in the deepest seawater on Earth and shed a new light on potential biological processes in this extreme environment.

Identifiants

pubmed: 30975208
doi: 10.1186/s40168-019-0652-3
pii: 10.1186/s40168-019-0652-3
pmc: PMC6460516
doi:

Substances chimiques

Bacterial Proteins 0
Hydrocarbons 0
RNA, Ribosomal, 16S 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

47

Références

Bioinformatics. 2006 Jul 1;22(13):1658-9
pubmed: 16731699
Bioinformatics. 2009 Jul 15;25(14):1754-60
pubmed: 19451168
Int J Syst Evol Microbiol. 2011 Feb;61(Pt 2):375-380
pubmed: 20305063
Proc Natl Acad Sci U S A. 2017 Oct 24;114(43):E8947-E8949
pubmed: 29073088
Proc Natl Acad Sci U S A. 2015 Nov 3;112(44):13591-6
pubmed: 26438854
Science. 2010 Jul 30;329(5991):559-62
pubmed: 20671186
Proc Natl Acad Sci U S A. 2009 Aug 4;106(31):12580-6
pubmed: 19617564
Proc Natl Acad Sci U S A. 2012 Dec 11;109(50):20292-7
pubmed: 21969552
Science. 2010 Oct 8;330(6001):208-11
pubmed: 20847236
PeerJ. 2015 Aug 27;3:e1165
pubmed: 26336640
Nucleic Acids Res. 2014 Jan;42(Database issue):D206-14
pubmed: 24293654
Appl Environ Microbiol. 2015 Dec;81(24):8265-76
pubmed: 26386059
Gigascience. 2012 Dec 27;1(1):18
pubmed: 23587118
Nat Commun. 2013;4:2304
pubmed: 23942190
ISME J. 2013 Dec;7(12):2315-29
pubmed: 23902988
Science. 2010 Oct 8;330(6001):204-8
pubmed: 20736401
Nat Methods. 2013 Oct;10(10):996-8
pubmed: 23955772
Front Microbiol. 2016 May 09;7:665
pubmed: 27242695
ISME J. 2013 Nov;7(11):2091-104
pubmed: 23788333
Front Microbiol. 2017 Jan 10;7:2131
pubmed: 28119669
Environ Microbiol. 2011 May;13(5):1168-78
pubmed: 21261799
Annu Rev Microbiol. 2002;56:289-314
pubmed: 12142488
Front Microbiol. 2016 Aug 10;7:1261
pubmed: 27559333
Environ Microbiol Rep. 2011 Aug;3(4):449-58
pubmed: 23761307
Science. 2017 Sep 1;357(6354):903-907
pubmed: 28860382
Nat Commun. 2014 Dec 12;5:5755
pubmed: 25502912
Proc Natl Acad Sci U S A. 2017 Jul 11;114(28):7432-7437
pubmed: 28652349
Nucleic Acids Res. 2010 Jul;38(12):e132
pubmed: 20403810
Bioinformatics. 2012 Jun 1;28(11):1420-8
pubmed: 22495754
PLoS One. 2018 Apr 5;13(4):e0195102
pubmed: 29621268
Mol Ecol. 2008 Sep;17(18):4092-106
pubmed: 19238708
ISME J. 2012 Sep;6(9):1715-27
pubmed: 22717885
Environ Microbiol. 2014 Jan;16(1):60-71
pubmed: 23826624
Appl Environ Microbiol. 2013 Oct;79(19):5962-9
pubmed: 23872556
Appl Environ Microbiol. 1996 Feb;62(2):316-22
pubmed: 8593035
Genome Res. 2015 Jul;25(7):1043-55
pubmed: 25977477
Genome Res. 2007 Mar;17(3):377-86
pubmed: 17255551
Microbiome. 2016 Jul 19;4(1):20
pubmed: 27391119
Antonie Van Leeuwenhoek. 2015 Jan;107(1):119-32
pubmed: 25326795
Proc Natl Acad Sci U S A. 2015 Mar 17;112(11):E1230-6
pubmed: 25713387

Auteurs

Jiwen Liu (J)

MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, 266003, China.
Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266237, China.

Yanfen Zheng (Y)

MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, 266003, China.

Heyu Lin (H)

MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, 266003, China.

Xuchen Wang (X)

Key Laboratory of Marine Chemistry Theory and Technology, Ministry of Education, Qingdao, 266100, China.

Meng Li (M)

Institute for Advanced Study, Shenzhen University, Shenzhen, 518060, China.

Yang Liu (Y)

Institute for Advanced Study, Shenzhen University, Shenzhen, 518060, China.

Meng Yu (M)

Key Laboratory of Marine Chemistry Theory and Technology, Ministry of Education, Qingdao, 266100, China.

Meixun Zhao (M)

Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266237, China.
Key Laboratory of Marine Chemistry Theory and Technology, Ministry of Education, Qingdao, 266100, China.

Nikolai Pedentchouk (N)

School of Environmental Sciences, University of East Anglia, Norwich, NR4 7TJ, UK.

David J Lea-Smith (DJ)

School of Biological Sciences, University of East Anglia, Norwich, NR4 7TJ, UK.

Jonathan D Todd (JD)

School of Biological Sciences, University of East Anglia, Norwich, NR4 7TJ, UK.

Clayton R Magill (CR)

Lyell Centre, Heriot-Watt University, Edinburgh, EH14 4AS, UK.

Wei-Jia Zhang (WJ)

Laboratory of Deep Sea Microbial Cell Biology, Institute of Deep Sea Science and Engineering, Chinese Academy of Sciences, Sanya, 572000, China.

Shun Zhou (S)

MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, 266003, China.

Delei Song (D)

MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, 266003, China.

Haohui Zhong (H)

MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, 266003, China.

Yu Xin (Y)

Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266237, China.
Key Laboratory of Marine Chemistry Theory and Technology, Ministry of Education, Qingdao, 266100, China.

Min Yu (M)

MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, 266003, China.
Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266237, China.

Jiwei Tian (J)

Key Laboratory of Physical Oceanography, Ministry of Education, Ocean University of China, Qingdao, 266100, China. tianjw@ouc.edu.cn.
Marine Dynamic Process and Climate Function Laboratory, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266237, China. tianjw@ouc.edu.cn.

Xiao-Hua Zhang (XH)

MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, 266003, China. xhzhang@ouc.edu.cn.
Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266237, China. xhzhang@ouc.edu.cn.

Articles similaires

Genome, Chloroplast Phylogeny Genetic Markers Base Composition High-Throughput Nucleotide Sequencing
Photosynthesis Ribulose-Bisphosphate Carboxylase Carbon Dioxide Molecular Dynamics Simulation Cyanobacteria
Animals Hemiptera Insect Proteins Phylogeny Insecticides
Populus Soil Microbiology Soil Microbiota Fungi

Classifications MeSH