Microbial community structure across the tree of life in the extreme Río Tinto

Abstract

Understanding biotic versus abiotic forces that shape community structure is a fundamental aim of microbial ecology. The acidic and heavy metal extreme Río Tinto (RT) in southwestern Spain provides a rare opportunity to conduct an ecosystem-wide biodiversity inventory at the level of all three domains of life, because diversity there is low and almost exclusively microbial. Despite improvements in high-throughput DNA sequencing, environmental biodiversity studies that use molecular metrics and consider entire ecosystems are rare. These studies can be prohibitively expensive if domains are considered separately, and differences in copy number of eukaryotic ribosomal RNA genes can bias estimates of relative abundances of phylotypes recovered. In this study we have overcome these barriers (1) by targeting all three domains in a single polymerase chain reaction amplification and (2) by using a replicated sampling design that allows for incidencebased methods to extract measures of richness and carry out downstream analyses that address community structuring effects. Our work showed that combined bacterial and archaeal richness is an order of magnitude higher than eukaryotic richness. We also found that eukaryotic richness was highest at the most extreme sites, whereas combined bacterial and archaeal richness was highest at less extreme sites. Quantitative community phylogenetics showed abiotic forces to be primarily responsible for shaping the RT community structure. Canonical correspondence analysis revealed co-occurrence of obligate symbionts and their putative hosts that may contribute to biotic forces shaping community structure and may further provide a possible mechanism for persistence of certain low-abundance bacteria encountered in the RT.

Community transcriptomics reveals unexpected high microbial diversity in acidophilic biofilm communities

“…Positive NTI values show phylogenetic clustering in all samples, indicating that taxa are more closely related at the tips of the phylogeny (Figure 4b). Positive NTI and negative NRI values have been observed in Rio Tinto AMD samples (Amaral-Zettler et al, 2011). Overall, the results suggest that the AMD system is characterized by a high diversity at the phylum level, but with relatively few closely related members of each phylum.…”

“…AMD systems are generally dominated by few acidophilic Bacteria belonging to the Nitrospira and Proteobacteria phyla, whereas lower abundance members include Firmicutes, Actinobacteria and Acidobacteria phyla, Archaea and Eukaryotes (for example, Druschel et al, 2004;Golyshina and Timmis, 2005;Baker et al, 2009;Amaral-Zettler et al, 2011;Garcia-Moyano et al, 2012;and reviewed by Johnson, 2012). Cultivation-independent techniques such as community genomics, proteomics, and microarrays have been successfully applied to study the physiology and ecology of acidophilic organisms in their natural environments.…”

Oxygen-dependent niche formation of a pyrite-dependent acidophilic consortium built by archaea and bacteria

“…Sequence analysis revealed the presence of clones most closely related to the ARMAN species described by Baker et al (2006) as well as clones belonging to the Thermoplasmatales. The detected ARMAN clones (ARMAN-Clone_HM_4-46% abundant; ARMAN-Clone_HM_7-50% and ARMAN-Clone_HM_29-4%) cluster in the ARMAN branch together with other uncultured archaea clones from the Rio Tinto (Amaral-Zettler et al, 2011). The Thermoplasmatales sequences are mainly related to a branch with uncultured representatives of this order, whereas one type (Archaea-Clone_HM_ 19-40% from all archaea clones) is related to Ferroplasma (Figure 5).…”

“…The more related sequences from uncultured organisms stem from other acidic environments like the Iberian Pyrite Belt, including Rio Tinto (Rowe et al, 2007;Amaral-Zettler et al, 2011;Gonzalez-Toril et al, 2011). Due to their remote position in the phylogenetic tree and as there is no isolated species belonging to these deeply branching organisms, it is not possible to assign certain physiological characteristics yet.…”

“…The Thermoplasmatales sequences are mainly related to a branch with uncultured representatives of this order, whereas one type (Archaea-Clone_HM_ 19-40% from all archaea clones) is related to Ferroplasma (Figure 5). The closest relatives to Archaea-Clone_HM_2 (42%), Archaea-Clone_ HM_20 (6%) and Archaea-Clone_HM_21 (13%) are so far uncultured representatives from other acidic environments found in the Iberian Pyrite Belt ( Figure 5) (Rowe et al, 2007;Amaral-Zettler et al, 2011;Gonzalez-Toril et al, 2011). Based on the restriction fragment length polymorphism results, more specific probes for the detection of ARMAN and Thermoplasmatales were used.…”