Evolution from a respiratory ancestor to fill syntrophic and fermentative niches: comparative fenomics of six Geobacteraceae species

Jessica E Butler,Nelson D Young,Derek R Lovley

doi:10.1186/1471-2164-10-103

Jessica E Butler, Nelson D Young + Show 1 more

Open Access

https://doi.org/10.1186/1471-2164-10-103

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Journal: BMC Genomics	Publication Date: Jan 1, 2009
Citations: 103	License type: cc-by

Affiliation: University of Massachusetts Amherst

Abstract

BackgroundThe anaerobic degradation of organic matter in natural environments, and the biotechnical use of anaerobes in energy production and remediation of subsurface environments, both require the cooperative activity of a diversity of microorganisms in different metabolic niches. The Geobacteraceae family contains members with three important anaerobic metabolisms: fermentation, syntrophic degradation of fermentation intermediates, and anaerobic respiration.ResultsIn order to learn more about the evolution of anaerobic microbial communities, the genome sequences of six Geobacteraceae species were analyzed. The results indicate that the last common Geobacteraceae ancestor contained sufficient genes for anaerobic respiration, completely oxidizing organic compounds with the reduction of external electron acceptors, features that are still retained in modern Geobacter and Desulfuromonas species. Evolution of specialization for fermentative growth arose twice, via distinct lateral gene transfer events, in Pelobacter carbinolicus and Pelobacter propionicus. Furthermore, P. carbinolicus gained hydrogenase genes and genes for ferredoxin reduction that appear to permit syntrophic growth via hydrogen production. The gain of new physiological capabilities in the Pelobacter species were accompanied by the loss of several key genes necessary for the complete oxidation of organic compounds and the genes for the c-type cytochromes required for extracellular electron transfer.ConclusionThe results suggest that Pelobacter species evolved parallel strategies to enhance their ability to compete in environments in which electron acceptors for anaerobic respiration were limiting. More generally, these results demonstrate how relatively few gene changes can dramatically transform metabolic capabilities and expand the range of environments in which microorganisms can compete.

Highlights

The anaerobic degradation of organic matter in natural environments, and the biotechnical use of anaerobes in energy production and remediation of subsurface environments, both require the cooperative activity of a diversity of microorganisms in different metabolic niches
The results suggest that Pelobacter species evolved parallel strategies to enhance their ability to compete in environments in which electron acceptors for anaerobic respiration were limiting
P. carbinolicus genes (Pcar_2989–Pcar2997) are only distantly related to the Geobacter and Desulfuromonas operons, but because they are similar to genes from a variety of species including D. acetoxidans, it is difficult to be confident about the lateral transfer source. These results provide insights into the evolution of Geobacteraceae species into different environmental niches and biotechnological applications

Summary

Introduction

The anaerobic degradation of organic matter in natural environments, and the biotechnical use of anaerobes in energy production and remediation of subsurface environments, both require the cooperative activity of a diversity of microorganisms in different metabolic niches. The global carbon cycle and the production of a number of biofuels depends on the cooperative interaction of a physiological diversity of anaerobic microorganisms These include microorganisms that ferment complex substrates to simpler molecules; respiratory microorganisms (page number not for citation purposes). In hydrocarbon-contaminated subsurface environments Geobacter species can play an important role in the bioremediation of aromatic hydrocarbons by oxidizing the contaminants with the reduction of Fe(III) oxides naturally present in the subsurface [3,4]. This is a process which can be artificially stimulated [5,6]. The ability of Geobacter and Desulfuromonas species to oxidize organic compounds with electron transfer to graphite electrodes provides a convenient method for harvesting electricity from aquatic sediments and organic wastes to power electronic devices [9,10,11]

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