Population level functional diversity in a microbial community revealed by comparative genomic and metagenomic analyses

Abstract

In microbial mat communities of Yellowstone hot springs, ribosomal RNA (rRNA) sequence diversity patterns indicate the presence of closely related bacterial populations along environmental gradients of temperature and light. To identify the functional bases for adaptation, we sequenced the genomes of two cyanobacterial (Synechococcus OS-A and OS-B 0 ) isolates representing ecologically distinct populations that dominate at different temperatures and are major primary producers in the mat. There was a marked lack of conserved large-scale gene order between the two Synechococcus genomes, indicative of extensive genomic rearrangements. Comparative genomic analyses showed that the isolates shared a large fraction of their gene content at high identity, yet, differences in phosphate and nitrogen utilization pathways indicated that they have adapted differentially to nutrient fluxes, possibly by the acquisition of genes by lateral gene transfer or their loss in certain populations. Comparisons of the Synechococcus genomes to metagenomic sequences derived from mats where these Synechococcus stains were originally isolated, revealed new facets of microbial diversity. First, Synechococcus populations at the lower temperature regions of the mat showed greater sequence diversity than those at high temperatures, consistent with a greater number of ecologically distinct populations at the lower temperature. Second, we found evidence of a specialized population that is apparently very closely related to Synechococcus OS-B 0 , but contains genes that function in the uptake of reduced ferrous iron. In situ expression studies demonstrated that these genes are differentially expressed over the diel cycle, with highest expression when the mats are anoxic and iron may be in the reduced state. Genomic information from these mat-specific isolates and metagenomic information can be coupled to detect naturally occurring populations that are associated with different functionalities, not always represented by isolates, but which may nevertheless be important for niche partitioning and the establishment of microbial community structure.

Microdiversity of extracellular enzyme genes among sequenced prokaryotic genomes

“…Martiny et al (2006) also found that the gene content for phosphate acquisition was not congruent with rRNA phylogeny for members of Prochlorococcus. Likewise, extremely close relatives of hot spring Synechococcus have been shown to differ in their adaptations to light levels (Becraft et al, 2011) as well as phosphorus and nitrogen use pathways (Bhaya et al, 2007). Isolates of Pseudomonas, Acinetobacter (Choudhary and Johri, 2011) and Brevundimonas (Jaspers and Overmann, 2004), which had identical 16S rRNA gene sequences, were also found to occupy different ecological niches, with each using a unique combination of carbon substrates.…”

“…This has been demonstrated for resource traits such as particle colonization (Hunt et al, 2008), light adaptation (Moore et al, 1998;West and Scanlan, 1999;Johnson et al, 2006;Becraft et al, 2011) and nutrient use (Jaspers and Overmann, 2004;Martiny et al, 2006;Bhaya et al, 2007;Choudhary and Johri, 2011). This fine-scale association appears to hold true across the prokaryotic domains for genetically simple carbon use traits (Martiny et al, 2012); however, it is unknown whether extracellular enzyme traits also follow this pattern.…”

Community ecology of hot spring cyanobacterial mats: predominant populations and their functional potential

“…Cluster-1 contained scaffolds that were strongly associated with the Synechococcus spp. strains A and B 0 genomes, and included cyanobacterial phylogenetic marker genes and functional genes that were indicative of oxygenic photosynthesis, the Calvin-BensonBassham cycle and genes involved in nitrogen and phosphorus acquisition that were described previously (Steunou et al, 2006(Steunou et al, , 2008Bhaya et al, 2007). Most (86%) of these metagenomic sequences were jointly recruited and were more closely related to either the Synechococcus sp.…”

“…The discovery of ferrous iron transporter homologs in Synechococcus sp. A-like populations (this study), and in B 0 -like populations (Bhaya et al, 2007), as well as the presence of these genes in the Roseiflexus sp. strain RS1 genome (van der Meer et al, 2010), suggests that the ability to use Fe 2 þ might be a common adaptation among the mat community members.…”

“…and Roseiflexus spp. isolates closely related to native mat populations (Allewalt et al, 2006;Bhaya et al, 2007;van der Meer et al, 2010).…”