Cellular adhesiveness and cellulolytic capacity in Anaerolineae revealed by omics-based genome interpretation

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Abstract

Background

The Anaerolineae lineage of Chloroflexi had been identified as one of the core microbial populations in anaerobic digesters; however, the ecological role of the Anaerolineae remains uncertain due to the scarcity of isolates and annotated genome sequences. Our previous metatranscriptional analysis revealed this prevalent population that showed minimum involvement in the main pathways of cellulose hydrolysis and subsequent methanogenesis in the thermophilic cellulose fermentative consortium (TCF).

Results

In further pursuit, five high-quality curated draft genomes (>98 % completeness) of this population, including two affiliated with the inaccessible lineage of SBR1031, were retrieved by sequence-based multi-dimensional coverage binning. Comparative genomic analyses revealed versatile genetic capabilities for carbohydrate-based fermentative lifestyle including key genes catalyzing cellulose hydrolysis in Anaerolinea phylotypes. However, the low transcriptional activities of carbohydrate-active genes (CAGs) excluded cellulolytic capability as the selective advantage for their prevalence in the community. Instead, a substantially active type VI pili (Tfp) assembly was observed. Expression of the tight adherence protein on the Tfp indicated its function for cellular attachment which was further testified to be more likely related to cell aggregation other than cellulose surface adhesion. Meanwhile, this Tfp structure was found not contributing to syntrophic methanogenesis. Members of the SBR1031 encoded key genes for acetogenic dehydrogenation that may allow ethanol to be used as a carbon source.

Conclusion

The common prevalence of Anaerolineae in anaerobic digesters should be originated from advantageous cellular adhesiveness enabled by Tfp assembly other than its potential as cellulose degrader or anaerobic syntrophs.

Electronic supplementary material

The online version of this article (doi:10.1186/s13068-016-0524-z) contains supplementary material, which is available to authorized users.

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Community structure and metabolism through reconstruction of microbial genomes from the environment.

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Microbial communities are vital in the functioning of all ecosystems; however, most microorganisms are uncultivated, and their roles in natural systems are unclear. Here, using random shotgun sequencing of DNA from a natural acidophilic biofilm, we report reconstruction of near-complete genomes of Leptospirillum group II and Ferroplasma type II, and partial recovery of three other genomes. This was possible because the biofilm was dominated by a small number of species populations and the frequency of genomic rearrangements and gene insertions or deletions was relatively low. Because each sequence read came from a different individual, we could determine that single-nucleotide polymorphisms are the predominant form of heterogeneity at the strain level. The Leptospirillum group II genome had remarkably few nucleotide polymorphisms, despite the existence of low-abundance variants. The Ferroplasma type II genome seems to be a composite from three ancestral strains that have undergone homologous recombination to form a large population of mosaic genomes. Analysis of the gene complement for each organism revealed the pathways for carbon and nitrogen fixation and energy generation, and provided insights into survival strategies in an extreme environment.

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Extracellular electron transfer via microbial nanowires.

Gemma Reguera, Kevin D. McCarthy, Teena Mehta … (2005)

Microbes that can transfer electrons to extracellular electron acceptors, such as Fe(iii) oxides, are important in organic matter degradation and nutrient cycling in soils and sediments. Previous investigations on electron transfer to Fe(iii) have focused on the role of outer-membrane c-type cytochromes. However, some Fe(iii) reducers lack c-cytochromes. Geobacter species, which are the predominant Fe(iii) reducers in many environments, must directly contact Fe(iii) oxides to reduce them, and produce monolateral pili that were proposed, on the basis of the role of pili in other organisms, to aid in establishing contact with the Fe(iii) oxides. Here we report that a pilus-deficient mutant of Geobacter sulfurreducens could not reduce Fe(iii) oxides but could attach to them. Conducting-probe atomic force microscopy revealed that the pili were highly conductive. These results indicate that the pili of G. sulfurreducens might serve as biological nanowires, transferring electrons from the cell surface to the surface of Fe(iii) oxides. Electron transfer through pili indicates possibilities for other unique cell-surface and cell-cell interactions, and for bioengineering of novel conductive materials.

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Is Open Access

IMG 4 version of the integrated microbial genomes comparative analysis system

Victor Markowitz, I-Min Chen, Krishna Palaniappan … (2013)

The Integrated Microbial Genomes (IMG) data warehouse integrates genomes from all three domains of life, as well as plasmids, viruses and genome fragments. IMG provides tools for analyzing and reviewing the structural and functional annotations of genomes in a comparative context. IMG’s data content and analytical capabilities have increased continuously since its first version released in 2005. Since the last report published in the 2012 NAR Database Issue, IMG’s annotation and data integration pipelines have evolved while new tools have been added for recording and analyzing single cell genomes, RNA Seq and biosynthetic cluster data. Different IMG datamarts provide support for the analysis of publicly available genomes (IMG/W: http://img.jgi.doe.gov/w), expert review of genome annotations (IMG/ER: http://img.jgi.doe.gov/er) and teaching and training in the area of microbial genome analysis (IMG/EDU: http://img.jgi.doe.gov/edu).

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Author and article information

Contributors

Yu Xia: shuixia100@gmail.com

Yubo Wang: yubo870508@163.com

Yi Wang: h1095106@connect.hku.hk

Francis Y. L. Chin: chin@cs.hku.hk

Tong Zhang: 852-28578551 , zhangt@hku.hk , zhangt@hkucc.hku.hk , http://web.hku.hk/~zhangt/ZhangT.htm

Journal

Journal ID (nlm-ta): Biotechnol Biofuels

Journal ID (iso-abbrev): Biotechnol Biofuels

Title: Biotechnology for Biofuels

Publisher: BioMed Central (London )

ISSN (Electronic): 1754-6834

Publication date (Electronic): 23 May 2016

Publication date PMC-release: 23 May 2016

Publication date Collection: 2016

Volume: 9

Electronic Location Identifier: 111

Affiliations

[ ]Shenzhen Institute of Research and Innovation, The University of Hong Kong, Shenzhen, China

[ ]Department of Civil Engineering, The University of Hong Kong, Hong Kong SAR, China

[ ]Department of Computer Science, The University of Hong Kong, Hong Kong SAR, China

[ ]Department of Computing, Hang Seng Management College, Hong Kong SAR, China

[ ]Environmental Biotechnology Lab, The University of Hong Kong, Pokfulam Road, Hong Kong, China

Article

Publisher ID: 524

DOI: 10.1186/s13068-016-0524-z

PMC ID: 4877987

PubMed ID: 27222666

SO-VID: 92fd1e7b-dacf-448e-a23d-189777c8184c

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 18 January 2016

Date accepted : 9 May 2016

Funding

Funded by: Shenzhen Municipal Science and Technology Innovation Council

Award ID: JCYJ20130401141412386

Award Recipient : Tong Zhang

Funded by: Hong Kong University Grants Committee

Award ID: HKU 7111/12E

Award Recipient : Francis Y. L. Chin

Custom metadata

ScienceOpen disciplines: Biotechnology

Keywords: cellular adhesion,aggregation,cellulolytic capacity,anaerolineae,chloroflexi,anaerolinales

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ScienceOpen disciplines: Biotechnology

Keywords: cellular adhesion, aggregation, cellulolytic capacity, anaerolineae, chloroflexi, anaerolinales

Cellular adhesiveness and cellulolytic capacity in Anaerolineae revealed by omics-based genome interpretation

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Abstract

Background

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Electronic supplementary material

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Most cited references 47

Community structure and metabolism through reconstruction of microbial genomes from the environment.

Extracellular electron transfer via microbial nanowires.

IMG 4 version of the integrated microbial genomes comparative analysis system

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