Abstract
A better understand the ecology of microbes and their role in the global ecosystem could be achieved if traditional ecological theories can be applied to microbes. In ecology organisms are defined as specialists or generalists according to the breadth of their niche. Spatial distribution is often used as a proxy measure of niche breadth; generalists have broad niches and a wide spatial distribution and specialists a narrow niche and spatial distribution. Previous studies suggest that microbial distribution patterns are contrary to this idea; a microbial generalist genus (Desulfobulbus) has a limited spatial distribution while a specialist genus (Methanosaeta) has a cosmopolitan distribution. Therefore, we hypothesise that this counter-intuitive distribution within generalist and specialist microbial genera is a common microbial characteristic. Using molecular fingerprinting the distribution of four microbial genera, two generalists, Desulfobulbus and the methanogenic archaea Methanosarcina, and two specialists, Methanosaeta and the sulfate-reducing bacteria Desulfobacter were analysed in sediment samples from along a UK estuary. Detected genotypes of both generalist genera showed a distinct spatial distribution, significantly correlated with geographic distance between sites. Genotypes of both specialist genera showed no significant differential spatial distribution. These data support the hypothesis that the spatial distribution of specialist and generalist microbes does not match that seen with specialist and generalist large organisms. It may be that generalist microbes, while having a wider potential niche, are constrained, possibly by intrageneric competition, to exploit only a small part of that potential niche while specialists, with far fewer constraints to their niche, are more capable of filling their potential niche more effectively, perhaps by avoiding intrageneric competition. We suggest that these counter-intuitive distribution patterns may be a common feature of microbes in general and represent a distinct microbial principle in ecology, which is a real challenge if we are to develop a truly inclusive ecology.
Highlights
In order to better understand the ecology of microbes and their role in the global ecosystem, it is essential to determine whether ecological ideas and theories that have been derived from studies on plants and animals are applicable to microbes [1,2,3,4]
Genotypes 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 [8,30,31,32]. These data challenge assumptions from traditional ecology that spatial distribution is a proxy measure of niche breadth leading us to propose the hypothesis that, in contrast to traditional ecological ideas, the breadth of the spatial distribution of specialist and generalist microbes is inversely related to the breadth of their potential niches
We show that within microbial genera metabolic flexibility appears to have a profound effect on the spatial distribution patterns of those genera, with members of metabolic generalist genera showing a narrower spatial distribution than metabolic specialist genera
Summary
In order to better understand the ecology of microbes and their role in the global ecosystem, it is essential to determine whether ecological ideas and theories that have been derived from studies on plants and animals are applicable to microbes [1,2,3,4]. 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 [8,30,31,32] These data challenge assumptions from traditional ecology that spatial distribution is a proxy measure of niche breadth leading us to propose the hypothesis that, in contrast to traditional ecological ideas, the breadth of the spatial distribution of specialist and generalist microbes is inversely related to the breadth of their potential niches. These data show that metabolic flexibility does appear to directly affect the distribution of microbial genera; metabolic generalists (Desulfobulbus and Methanosarcina) have a specialist spatial distribution strongly correlated with environmental variables and metabolic specialists (Methanosaeta and Desulfobacter) have a generalist spatial distribution along an estuarine gradient that is not correlated to environmental factors
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