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Metabolic streamlining in an open-ocean nitrogen-fixing cyanobacterium

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Abstract

Nitrogen (N2)-fixing marine cyanobacteria are an important source of fixed inorganic nitrogen that supports oceanic primary productivity and carbon dioxide removal from the atmosphere1. A globally distributed2,3, periodically abundant4 N2-fixing5 marine cyanobacterium, UCYN-A, was recently found to lack the oxygen-producing photosystem II complex6 of the photosynthetic apparatus, indicating a novel metabolism, but remains uncultivated. Here we show, from metabolic reconstructions inferred from the assembly of the complete UCYN-A genome using massively parallel pyrosequencing of paired-end reads, that UCYN-A has a photofermentative metabolism and is dependent on other organisms for essential compounds. We found that UCYN-A lacks a number of major metabolic pathways including the tricarboxylic acid cycle, but retains sufficient electron transport capacity to generate energy and reducing power from light. Unexpectedly, UCYN-A has a reduced genome (1.44 megabases) that is structurally similar to many chloroplasts and some bacteria, in that it contains inverted repeats of ribosomal RNA operons7. The lack of biosynthetic pathways for several amino acids and purines suggests that this organism depends on other organisms, either in close association or in symbiosis, for critical nutrients. However, size fractionation experiments using natural populations have so far not provided evidence of a symbiotic association with another microorganism. The UCYN-A cyanobacterium is a paradox in evolution and adaptation to the marine environment, and is an example of the tight metabolic coupling between microorganisms in oligotrophic oceanic microbial communities.

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Figure 1: Circular map of UCYN-A chromosome compared with Cyanothece sp. ATCC 51142.
Figure 2: Overview of the metabolism of UCYN-A.
Figure 3: Putative electron flows in UCYN-A.
Figure 4: UCYN-A nifH gene copies recovered by size fraction.

Accession codes

Data deposits

The UCYN-A genome reported here has been deposited at GenBank under accession code CP001842.

Change history

  • 04 March 2010

    'Trichloroacetic’ was replaced by ‘tricarboxylic’ in two instances on 4 March 2010.

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Acknowledgements

This work was supported by the Gordon and Betty Moore Foundation, the US National Science Foundation (NSF) and the NSF Center for Microbial Oceanography: Research and Education. 454 Life Sciences, a Roche Company, provided sequencing services. Flow cytometry was done by B. Carter in the Microbial Environmental Genomics Applications: Modelling, Experimentation, and Remote Sensing (MEGAMER) facility of the University of California, Santa Cruz. We thank I. Hewson for sample collection and preliminary metagenomic analysis.

Author Contributions J.P.Z. and J.P.A. designed the study. H.J.T. devised the genome-closing strategy, annotated the genome, performed all metabolic reconstructions, performed the metagenomic and metatranscriptomic analysis and wrote the manuscript with J.P.Z. S.R.B. prepared DNA for sequencing and assisted in genome assembly and closing. F.N. prepared paired-end libraries and sequenced the DNA. K.A.T. performed all PCR reactions relating to genome closure and confirmation of two genome orientations. B.A.D. performed the initial genome assembly. R.A.F. performed the size fractionation experiment.

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Correspondence to Jonathan P. Zehr.

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Competing interests

Brian A. Desany, Faheem Niazi, and Jason P. Affourtit are employees of 454 Life Sciences, A Roche Company, which provided sequencing services and software for this paper.

Supplementary information

Supplementary Information

This file contains Supplementary Methods, Supplementary Tables S1-S4, Supplementary Figures S1-S5 with Legends, Supplementary Notes and Supplementary References. (PDF 1215 kb)

Supplementary Data 1

This file contains the results of the comparison of the UCYN-A biosynthetic capacity for amino acids and purines to that of Cyanothece sp. ATCC51142. (XLS 49 kb)

Supplementary Data 2

This file contains the detail supporting the metagenomic and metatranscriptomic statistics in Table 1 of the main text. (XLS 192 kb)

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Tripp, H., Bench, S., Turk, K. et al. Metabolic streamlining in an open-ocean nitrogen-fixing cyanobacterium. Nature 464, 90–94 (2010). https://doi.org/10.1038/nature08786

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