Please wait a minute...
Submit  |   Chinese  | 
 
Advanced Search
   Home  |  Online Now  |  Current Issue  |  Focus  |  Archive  |  For Authors  |  Journal Information   Open Access  
Submit  |   Chinese  | 
Engineering    2019, Vol. 5 Issue (3) : 498 -504     https://doi.org/10.1016/j.eng.2019.01.011
Research Deep Matter & Energy—Article |
Core Metabolic Features and Hot Origin of Bathyarchaeota
Xiaoyuan Fenga, Yinzhao Wanga, Rahul Zubina, Fengping Wangab()
a State Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China
b State Key Laboratory of Ocean Engineering, Shanghai Jiao Tong University, Shanghai 200240, China
Abstract
Abstract  Abstract

The archaeal phylum Bathyarchaeota comprises highly diversified subgroups and is considered to be one of the most abundant microorganisms on earth. The metabolic features and evolution of this phylum still remain largely unknown. In this article, a comparative metabolic analysis of 15 newly reconstructed and 36 published metagenomic assembled genomes (MAGs) spanning 10 subgroups was performed, revealing the core metabolic features of Bathyarchaeota—namely, protein, lipid, and benzoate degradation; glycolysis; and the Wood–Ljungdahl (WL) pathway, indicating an acetyl-CoA-centralized metabolism within this phylum. Furthermore, a partial tricarboxylic acid (TCA) cycle, acetogenesis, and sulfur-related metabolic pathways were found in specific subgroups, suggesting versatile metabolic capabilities and ecological functions of different subgroups. Intriguingly, most of the MAGs from the Bathy-21 and -22 subgroups, which are placed at the phylogenetic root of all bathyarchaeotal lineages and likely represent the ancient Bathyarchaeota types, were found in hydrothermal environments and encoded reverse gyrase, suggesting a hyperthermophilic feature. This work reveals the core metabolic features of Bathyarchaeota, and indicates a hot origin of this archaeal phylum.

Keywords Bathyarchaeota      Metagenomics      Comparative genomics      Hyperthermophilic adaptation     
Corresponding Authors: Fengping Wang   
Issue Date: 11 July 2019
Service
E-mail this article
E-mail Alert
RSS
Articles by authors
Xiaoyuan Feng
Yinzhao Wang
Rahul Zubin
Fengping Wang
Cite this article:   
Xiaoyuan Feng,Yinzhao Wang,Rahul Zubin, et al. Core Metabolic Features and Hot Origin of Bathyarchaeota[J]. Engineering, 2019, 5(3): 498 -504 .
URL:  
http://www.engineering.org.cn/EN/10.1016/j.eng.2019.01.011     OR     http://www.engineering.org.cn/EN/Y2019/V5/I3/498
References
[1]   K. Kubo, K.G. Lloyd, J.F. Biddle, R. Amann, A. Teske, K. Knittel. Archaea of the Miscellaneous Crenarchaeotal Group are abundant, diverse and widespread in marine sediments. ISME J. 2012; 6(10): 1949-1965.
[2]   K.G. Lloyd, L. Schreiber, D.G. Petersen, K.U. Kjeldsen, M.A. Lever, A.D. Steen, et al.. Predominant Archaea in marine sediments degrade detrital proteins. Nature. 2013; 496(7444): 215-218.
[3]   J. Meng, J. Xu, D. Qin, Y. He, X. Xiao, F. Wang. Genetic and functional properties of uncultivated MCG Archaea assessed by metagenome and gene expression analyses. ISME J. 2014; 8(3): 650-659.
[4]   Y. He, M. Li, V. Perumal, X. Feng, J. Fang, J. Xie, et al.. Genomic and enzymatic evidence for acetogenesis among multiple lineages of the archaeal phylum Bathyarchaeota widespread in marine sediments. Nat Microbiol. 2016; 1(6): 16035.
[5]   X. Xiang, R. Wang, H. Wang, L. Gong, B. Man, Y. Xu. Distribution of Bathyarchaeota communities across different terrestrial settings and their potential ecological functions. Sci Rep. 2017; 7(1): 45028.
[6]   J.C. Fry, R.J. Parkes, B.A. Cragg, A.J. Weightman, G. Webster. Prokaryotic biodiversity and activity in the deep subseafloor biosphere. FEMS Microbiol Ecol. 2008; 66(2): 181-196.
[7]   Q. Li, F. Wang, Z. Chen, X. Yin, X. Xiao. Stratified active archaeal communities in the sediments of Jiulong River estuary, China. Front Microbiol. 2012; 3: 311.
[8]   Z. Zhou, J. Pan, F. Wang, J.D. Gu, M. Li. Bathyarchaeota: globally distributed metabolic generalists in anoxic environments. FEMS Microbiol Rev. 2018; 42(5): 639-655.
[9]   C.S. Lazar, B.J. Baker, K. Seitz, A.S. Hyde, G.J. Dick, K.U. Hinrichs, et al.. Genomic evidence for distinct carbon substrate preferences and ecological niches of Bathyarchaeota in estuarine sediments. Environ Microbiol. 2016; 18(4): 1200-1211.
[10]   W. Zhang, W. Ding, B. Yang, R. Tian, S. Gu, H. Luo, et al.. Genomic and transcriptomic evidence for carbohydrate consumption among microorganisms in a cold seep brine pool. Front Microbiol. 2016; 7: 1825.
[11]   T. Yu, W. Wu, W. Liang, M.A. Lever, K.U. Hinrichs, F. Wang. Growth of sedimentary Bathyarchaeota on lignin as an energy source. Proc Natl Acad Sci USA. 2018; 115(23): 6022-6027.
[12]   P.N. Evans, D.H. Parks, G.L. Chadwick, S.J. Robbins, V.J. Orphan, S.D. Golding, et al.. Methane metabolism in the archaeal phylum Bathyarchaeota revealed by genome-centric metagenomics. Science. 2015; 350(6259): 434-438.
[13]   W.F. Martin, F.L. Sousa, N. Lane. Energy at life’s origin. Science. 2014; 344(6188): 1092-1093.
[14]   M. Fillol, J.C. Auguet, E.O. Casamayor, C.M. Borrego. Insights in the ecology and evolutionary history of the Miscellaneous Crenarchaeotic Group lineage. ISME J. 2016; 10(3): 665-677.
[15]   Y. Peng, H.C. Leung, S.M. Yiu, F.Y. Chin. IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics. 2012; 28(11): 1420-1428.
[16]   B. Langmead, S.L. Salzberg. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012; 9(4): 357-359.
[17]   H. Li, B. Handsaker, A. Wysoker, T. Fennell, J. Ruan, N. Homer, et al.. The sequence alignment/map format and SAMtools. Bioinformatics. 2009; 25(16): 2078-2079.
[18]   D.D. Kang, J. Froula, R. Egan, Z. Wang. MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities. PeerJ. 2015; 3: e1165.
[19]   G.J. Dick, A.F. Andersson, B.J. Baker, S.L. Simmons, B.C. Thomas, A.P. Yelton, et al.. Community-wide analysis of microbial genome sequence signatures. Genome Biol. 2009; 10(8): R85.
[20]   M. Albertsen, P. Hugenholtz, A. Skarshewski, K.L. Nielsen, G.W. Tyson, P.H. Nielsen. Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes. Nat Biotechnol. 2013; 31(6): 533-538.
[21]   D.H. Parks, M. Imelfort, C.T. Skennerton, P. Hugenholtz, G.W. Tyson. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015; 25(7): 1043-1055.
[22]   K. Anantharaman, C.T. Brown, L.A. Hug, I. Sharon, C.J. Castelle, A.J. Probst, et al.. Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system. Nat Commun. 2016; 7(1): 13219.
[23]   N. Dombrowski, K.W. Seitz, A.P. Teske, B.J. Baker. Genomic insights into potential interdependencies in microbial hydrocarbon and nutrient cycling in hydrothermal sediments. Microbiome. 2017; 5(1): 106.
[24]   C.N. Butterfield, Z. Li, P.F. Andeer, S. Spaulding, B.C. Thomas, A. Singh, et al.. Proteogenomic analyses indicate bacterial methylotrophy and archaeal heterotrophy are prevalent below the grass root zone. PeerJ. 2016; 4: e2687.
[25]   S.P. Jungbluth, T. Glavina del Rio. Tringe SG, Stepanauskas R, Rappé MS. Genomic comparisons of a bacterial lineage that inhabits both marine and terrestrial deep subsurface systems. PeerJ. 2017; 5: e3134.
[26]   D.H. Parks, C. Rinke, M. Chuvochina, P.A. Chaumeil, B.J. Woodcroft, P.N. Evans, et al.. Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life. Nat Microbiol. 2017; 2(11): 1533-1542.
[27]   E. Pruesse, C. Quast, K. Knittel, B.M. Fuchs, W. Ludwig, J. Peplies, et al.. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 2007; 35(21): 7188-7196.
[28]   L. Fu, B. Niu, Z. Zhu, S. Wu, W. Li. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics. 2012; 28(23): 3150-3152.
[29]   K. Katoh, K. Misawa, K. Kuma, T. Miyata. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002; 30(14): 3059-3066.
[30]   A. Stamatakis. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014; 30(9): 1312-1313.
[31]   I. Letunic, P. Bork. Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res. 2011; 39(Suppl 2): W475-W478.
[32]   D. Hyatt, G.L. Chen, P.F. Locascio, M.L. Land, F.W. Larimer, L.J. Hauser. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinf. 2010; 11(1): 119.
[33]   M. Kanehisa, S. Goto. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res. 2000; 28(1): 27-30.
[34]   R.L. Tatusov, N.D. Fedorova, J.D. Jackson, A.R. Jacobs, B. Kiryutin, E.V. Koonin, et al.. The COG database: an updated version includes eukaryotes. BMC Bioinf. 2003; 4(1): 41.
[35]   N.D. Rawlings, M. Waller, A.J. Barrett, A. Bateman. MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res. 2014; 42(D1): D503-D509.
[36]   V. Lombard, H. Golaconda Ramulu, E. Drula, P.M. Coutinho, B. Henrissat. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 2014; 42(D1): D490-D495.
[37]   P.G. Bagos, K.D. Tsirigos, S.K. Plessas, T.D. Liakopoulos, S.J. Hamodrakas. Prediction of signal peptides in Archaea. Protein Eng Des Sel. 2009; 22(1): 27-35.
[38]   R. Sorek, Y. Zhu, C.J. Creevey, M.P. Francino, P. Bork, E.M. Rubin. Genome-wide experimental determination of barriers to horizontal gene transfer. Science. 2007; 318(5855): 1449-1452.
[39]   M. Csurös. Count: evolutionary analysis of phylogenetic profiles with parsimony and likelihood. Bioinformatics. 2010; 26(15): 1910-1912.
[40]   C.S. Lazar, J.F. Biddle, T.B. Meador, N. Blair, K.U. Hinrichs, A.P. Teske. Environmental controls on intragroup diversity of the uncultured benthic Archaea of the Miscellaneous Crenarchaeotal Group lineage naturally enriched in anoxic sediments of the White Oak River estuary (North Carolina, USA). Environ Microbiol. 2015; 17(7): 2228-2238.
[41]   S.G. Wakeham, C. Lee, J.I. Hedges, P.J. Hernes, M.J. Peterson. Molecular indicators of diagenetic status in marine organic matter. Geochim Cosmochim Acta. 1997; 61(24): 5363-5369.
[42]   V.B. Heuer, J.W. Pohlman, M.E. Torres, M. Elvert, K.U. Hinrichs. The stable carbon isotope biogeochemistry of acetate and other dissolved carbon species in deep subseafloor sediments at the northern Cascadia Margin. Geochim Cosmochim Acta. 2009; 73(11): 3323-3336.
[43]   L.M. Seyler, L.M. McGuinness, L.J. Kerkhof. Crenarchaeal heterotrophy in salt marsh sediments. ISME J. 2014; 8(7): 1534-1543.
[44]   T. Yu, Q. Liang, M. Niu, F. Wang. High occurrence of Bathyarchaeota (MCG) in the deep-sea sediments of South China Sea quantified using newly designed PCR primers. Environ Microbiol Rep. 2017; 9(4): 374-382.
[45]   M.A. Lever, V.B. Heuer, Y. Morono, N. Masui, F. Schmidt, M.J. Alperin, et al.. Acetogenesis in deep subseafloor sediments of the Juan de Fuca Ridge Flank: a synthesis of geochemical, thermodynamic, and gene-based evidence. Geomicrobiol J. 2010; 27(2): 183-211.
[46]   K. Richter, M. Haslbeck, J. Buchner. The heat shock response: life on the verge of death. Mol Cell. 2010; 40(2): 253-266.
[47]   A. Spang, E.F. Caceres. Ettema TJG. Genomic exploration of the diversity, ecology, and evolution of the archaeal domain of life. Science. 2017; 357(6351): eaaf3883.
Related
No related articles found!
Copyright © 2015 Higher Education Press & Engineering Sciences Press, All Rights Reserved.
京ICP备11030251号-2

 Engineering