Genotypic Distribution of a Specialist Model Microorganism, Methanosaeta, along an Estuarine Gradient: Does Metabolic Restriction Limit Niche Differentiation Potential?

Abstract

A reductionist ecological approach of using a model genus was adopted in order to understand how microbial community structure is driven by metabolic properties. The distribution along an estuarine gradient of the highly specialised genus Methanosaeta was investigated and compared to the previously determined distribution of the more metabolically flexible Desulfobulbus. Methanosaeta genotypic distribution along the Colne estuary (Essex, UK) was determined by DNA- and RNA-based denaturing gradient gel electrophoresis and 16S rRNA gene sequence analyses. Methanosaeta distribution was monotonic, with a consistently diverse community and no apparent niche partitioning either in DNA or RNA analyses. This distribution pattern contrasts markedly with the previously described niche partitioning and sympatric differentiation of the model generalist, Desulfobulbus. To explain this difference, it is hypothesised that Methanosaeta's strict metabolic needs limit its adaptation potential, thus populations do not partition into spatially distinct groups and so do not appear to be constrained by gross environmental factors such as salinity. Thus, at least for these two model genera, it appears that metabolic flexibility may be an important factor in spatial distribution and this may be applicable to other microbes.

Metabolic Flexibility as a Major Predictor of Spatial Distribution in Microbial Communities

“…While all Mantel tests were significant for Methanosaeta ( p <0.05) no coherent correlation could be seen with partial Mantel tests. Importantly, DNA- and RNA-based Desulfobulbus distribution patterns were very similar, as observed previously for Methanosaeta [30]. This implies that detected genotypes (from analysis of DNA) are active (from analysis of RNA), and thus DNA based DGGE fingerprints represent a satisfactory representation of metabolically active populations.…”

“…Banding patterns in the RNA-DGGE analysis of both Desulfobulbus and Methanosaeta (Figure S5) were very similar to those seen in the DNA-DGGE (Figure 1 and Figure S3). As with DNA-DGGE Desulfobulbus had a restricted pattern of spatial distribution, while Methanosaeta genotypes were constantly detected all along the estuary [30]. Cluster analyses showed spatially coherent clustering for Desulfobulbus clusters (Fig 3A) and a weak but inconsistent clustering for Methanosaeta (Fig 3B).…”

“…The model genera were the sulfate-reducing bacteria Desulfobulbus , a generalist genus that can respire both sulfur and nitrogen oxyanions, use fermentation for growth and metabolise a range of carbon sources [27], [28] and the methanogenic archaeal genus Methanosaeta , a metabolic specialist that uses acetate as both electron acceptor and donor and as its sole carbon source [29]. Genotypes (at approximately the species level) of the generalist Desulfobulbus genus were spatially restricted to distinct regions of the estuarine salinity gradient in a manner similar to that classically described for estuarine macrofauna [17] while genotypes of the specialist Methanosaeta showed no such differential distribution and were monotonically distributed along the estuary [8], [30]–[32].…”

Archaeal community diversity and abundance changes along a natural salinity gradient in estuarine sediments

“…Recently, specific mcr A and 16S rRNA gene primers and repeated PCR amplifications have been used to study the ecology of Methanosaeta in the Colne Estuary (Carbonero et al. , 2012; Oakley et al. , 2012).…”

An Unexpectedly Broad Thermal and Salinity-Tolerant Estuarine Methanogen Community

“…Estuaries play a unique interconnecting role between the terrestrial and marine environment [ 18 ]. They have been used to study the influence of environmental perturbation on in situ microbial community diversity, and function for specific microbial processes, including methanogenesis [ 19 , 20 , 21 ] and methanotrophy [ 18 ]. Interest is often primarily because, along with fjords and shallow coastal areas, estuaries are thought to contribute up to 75% of the marine global flux of methane to the atmosphere [ 22 ], despite making up only 16% of the total ocean surface area [ 23 ].…”