Community Structure and Function of High-Temperature Chlorophototrophic Microbial Mats Inhabiting Diverse Geothermal Environments

Christian G Klatt,Markus J Herrgard,Scott R Miller,Zackary J Jay,Sarah M Boomer,William P Inskeep,Douglas B Rusch,David M Ward,Susannah G Tringe,M Niki Parenteau,Donald A Bryant

doi:10.3389/fmicb.2013.00106

Abstract

Six phototrophic microbial mat communities from different geothermal springs (YNP) were studied using metagenome sequencing and geochemical analyses. The primary goals of this work were to determine differences in community composition of high-temperature phototrophic mats distributed across the Yellowstone geothermal ecosystem, and to identify metabolic attributes of predominant organisms present in these communities that may correlate with environmental attributes important in niche differentiation. Random shotgun metagenome sequences from six phototrophic communities (average ∼53 Mbp/site) were subjected to multiple taxonomic, phylogenetic, and functional analyses. All methods, including G + C content distribution, MEGAN analyses, and oligonucleotide frequency-based clustering, provided strong support for the dominant community members present in each site. Cyanobacteria were only observed in non-sulfidic sites; de novo assemblies were obtained for Synechococcus-like populations at Chocolate Pots (CP_7) and Fischerella-like populations at White Creek (WC_6). Chloroflexi-like sequences (esp. Roseiflexus and/or Chloroflexus spp.) were observed in all six samples and contained genes involved in bacteriochlorophyll biosynthesis and the 3-hydroxypropionate carbon fixation pathway. Other major sequence assemblies were obtained for a Chlorobiales population from CP_7 (proposed family Thermochlorobacteriaceae), and an anoxygenic, sulfur-oxidizing Thermochromatium-like (Gamma-proteobacteria) population from Bath Lake Vista Annex (BLVA_20). Additional sequence coverage is necessary to establish more complete assemblies of other novel bacteria in these sites (e.g., Bacteroidetes and Firmicutes); however, current assemblies suggested that several of these organisms play important roles in heterotrophic and fermentative metabolisms. Definitive linkages were established between several of the dominant phylotypes present in these habitats and important functional processes such as photosynthesis, carbon fixation, sulfur oxidation, and fermentation.

Highlights

Many naturally occurring microorganisms have eluded isolation, due in part to a poor understanding of the chemical, physical, and biotic factors defining their realized niches (Rappé and Giovannoni, 2003)
The six sites investigated in this study are representative of three general types of geothermal springs in Yellowstone National Park that support bacterial chlorophototrophic communities and include (i) alkaline-siliceous chloride springs, (ii) sulfidic-carbonate springs, and (iii) mildly acidic non-sulfidic springs containing high aqueous Fe(II) (e.g., CP_7) (Rowe et al, 1973; McClesky et al, 2005)
The major physical and geochemical constraints that have been postulated to control the distribution of phototrophs in these thermal springs are pH, temperature, sulfide concentration, and gradients in light and/or other chemicals existing as a function of mat depth (Brock, 1967, 1978; Cox et al, 2011; Boyd et al, 2012)

Summary

Introduction

Many naturally occurring microorganisms have eluded isolation, due in part to a poor understanding of the chemical, physical, and biotic factors defining their realized niches (Rappé and Giovannoni, 2003). Random shotgun sequencing of environmental DNA provides a direct and potentially less biased view of the composition and functional attributes of microbial communities. Three new chlorophototrophic organisms (i.e., organisms capable of (bacterio)chlorophyll-based phototrophy) were discovered in prior metagenome analyses of oxygenic mats in YNP, two of which lie outside the clades of known phototrophic organisms www.frontiersin.org. High-temperature chlorophototrophic microbial mats in the Chlorobiales and Chloroflexi (Klatt et al, 2011). Metagenome sequencing and subsequent bioinformatic analyses provide an opportunity to identify the metabolic attributes of uncultivated organisms that can be used to postulate detailed biochemical linkages among individual community members necessary for the development of computational models describing microbial interaction and community function (Taffs et al, 2009)

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