Comparative Genomics Unravels the Functional Roles of Co-occurring Acidophilic Bacteria in Bioleaching Heaps

Xian Zhang,Hongwei Liu,Xueduan Liu,Bo Miao,Xue Guo,Yunhua Xiao,Deliang Peng,Wenkun Huang,Yili Liang,Huaqun Yin,Liyuan Ma

doi:10.3389/fmicb.2017.00790

Abstract

The spatial-temporal distribution of populations in various econiches is thought to be potentially related to individual differences in the utilization of nutrients or other resources, but their functional roles in the microbial communities remain elusive. We compared differentiation in gene repertoire and metabolic profiles, with a focus on the potential functional traits of three commonly recognized members (Acidithiobacillus caldus, Leptospirillum ferriphilum, and Sulfobacillus thermosulfidooxidans) in bioleaching heaps. Comparative genomics revealed that intra-species divergence might be driven by horizontal gene transfer. These co-occurring bacteria shared a few homologous genes, which significantly suggested the genomic differences between these organisms. Notably, relatively more genes assigned to the Clusters of Orthologous Groups category [G] (carbohydrate transport and metabolism) were identified in Sulfobacillus thermosulfidooxidans compared to the two other species, which probably indicated their mixotrophic capabilities that assimilate both organic and inorganic forms of carbon. Further inspection revealed distinctive metabolic capabilities involving carbon assimilation, nitrogen uptake, and iron-sulfur cycling, providing robust evidence for functional differences with respect to nutrient utilization. Therefore, we proposed that the mutual compensation of functionalities among these co-occurring organisms might provide a selective advantage for efficiently utilizing the limited resources in their habitats. Furthermore, it might be favorable to chemoautotrophs' lifestyles to form mutualistic interactions with these heterotrophic and/or mixotrophic acidophiles, whereby the latter could degrade organic compounds to effectively detoxify the environments. Collectively, the findings shed light on the genetic traits and potential metabolic activities of these organisms, and enable us to make some inferences about genomic and functional differences that might allow them to co-exist.

Highlights

Unraveling the ecological and functional roles of microorganisms in biological communities is an important but still elusive issue (Prosser et al, 2007), even though these microbes are thought to be crucial to the function ecosystems (Harris, 2009; Jiao et al, 2010; Hua et al, 2015)
The GC contents of the A. caldus genomes were much higher; a plausible explanation for this finding is that the optimal growth temperature (Topt) is regarded as one of the environmental factors that positively influences genomic GC content in prokaryotes (Musto et al, 2004, 2006) given that A. caldus is the primary sulfur oxidizer in bioleaching operations at temperatures above 40◦C (Acuña et al, 2013)
The GC contents of the bacterial genomes varied dramatically, and they were influenced by multiple factors (Hildebrand et al, 2010), such as genome size (Bentley and Parkhill, 2004), environment (Foerstner et al, 2005), nitrogen utilization (Mcewan et al, 1998), and aerobiosis (Naya et al, 2002)

Summary

Introduction

Unraveling the ecological and functional roles of microorganisms in biological communities is an important but still elusive issue (Prosser et al, 2007), even though these microbes are thought to be crucial to the function ecosystems (Harris, 2009; Jiao et al, 2010; Hua et al, 2015). As stated by Sogin et al (2006), there is a surprisingly wide biodiversity of microbial communities in pristine environments. Similar results were generally observed in other natural and anthropogenic environments based on metagenomic and metatranscriptomic analyses (Chen et al, 2015; Goltsman et al, 2015; Xiao et al, 2016; Zhang et al, 2016d). Genomes of microbial members in various communities have been reconstructed with the benefit of cultivation-independent sequencing (Tyson et al, 2004; Mason et al, 2012; Wu et al, 2016), providing a first glimpse of their functional roles in situ. Several bioinformatics-based strategies have been attempted to obtain genomic assemblies from metagenomic datasets (Dick et al, 2009; Hua et al, 2015). Considerable efforts have been made to expand the scope of microbial genetics and ecophysiology on a global scale; relatively little is known about how these populations co-exist within the same microbial community

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Conclusion