Abstract
Nitrogen is crucially limiting in ocean surface waters, and its availability varies substantially with coastal regions typically richer in nutrients than open oceans. In a biological stoichiometry framework, a parsimonious strategy of nitrogen allocation predicts nitrogen content of proteins to be lower in communities adapted to open ocean than to coastal regions. To test this hypothesis we have directly interrogated marine microbial communities, using a series of metagenomics datasets with a broad geographical distribution from the Global Ocean Sampling Expedition. Analyzing over 20 million proteins, we document a ubiquitous signal of nitrogen conservation in open ocean communities, both in membrane and non-membrane proteins. Efficient nitrogen allocation is expected to specifically target proteins that are expressed at high rate in response to nitrogen starvation. Furthermore, in order to preserve protein functional efficiency, economic nitrogen allocation is predicted to target primarily the least functionally constrained regions of proteins. Contrasting the NtcA-induced pathway, typically up-regulated in response to nitrogen starvation, with the arginine anabolic pathway, which is instead up-regulated in response to nitrogen abundance, we show how both these predictions are fulfilled. Using evolutionary rates as an informative proxy of functional constraints, we show that variation in nitrogen allocation between open ocean and coastal communities is primarily localized in the least functionally constrained regions of the genes triggered by NtcA. As expected, such a pattern is not detectable in the genes involved in the arginine anabolic pathway. These results directly link environmental nitrogen availability to different adaptive strategies of genome evolution, and emphasize the relevance of the material costs of evolutionary change in natural ecosystems.
Highlights
Recent investigations in “stoichiogenomics,” projecting biological stoichiometry into molecular evolution, have indicated that the atomic composition of proteins and genes has adaptive significance
We have found that protein nitrogen content is lower in communities adapted to oligotrophic open oceans in both membrane and non-membrane proteins
In order to have a relevant impact on the total nitrogen budget, an adaptive strategy of thrifty nitrogen allocation predicts that the largest difference between open ocean and coastal communities will be in genes up-regulated in response to nitrogen limitation
Summary
Recent investigations in “stoichiogenomics,” projecting biological stoichiometry into molecular evolution, have indicated that the atomic composition of proteins and genes has adaptive significance (reviewed in Elser et al, 2011). These studies have explored the material cost of evolutionary change, showing how environmental nutrient limitations have affected the Nitrogen Limitation in Open Oceans composition of the genetic material (Baudouin-Cornu et al, 2004; Bragg and Hyder, 2004; Bragg et al, 2006; Elser et al, 2006; Bragg and Wagner, 2007, 2009; Acquisti et al, 2009a,b; Gilbert and Fagan, 2011; Read et al, 2017). The aim of this paper is to bridge this gap, and to directly quantify the role of selection for nitrogen conservation in a natural ecosystem, combining the power of metagenomics and biogeochemistry in an evolutionary framework
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