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Ecological genomics of mutualism decline in nitrogen-fixing bacteria.

ABSTRACT: Anthropogenic changes can influence mutualism evolution; however, the genomic regions underpinning mutualism that are most affected by environmental change are generally unknown, even in well-studied model mutualisms like the interaction between legumes and their nitrogen (N)-fixing rhizobia. Such genomic information can shed light on the agents and targets of selection maintaining cooperation in nature. We recently demonstrated that N-fertilization has caused an evolutionary decline in mutualistic partner quality in the rhizobia that form symbiosis with clover. Here, population genomic analyses of N-fertilized versus control rhizobium populations indicate that evolutionary differentiation at a key symbiosis gene region on the symbiotic plasmid (pSym) contributes to partner quality decline. Moreover, patterns of genetic variation at selected loci were consistent with recent positive selection within N-fertilized environments, suggesting that N-rich environments might select for less beneficial rhizobia. By studying the molecular population genomics of a natural bacterial population within a long-term ecological field experiment, we find that: (i) the N environment is indeed a potent selective force mediating mutualism evolution in this symbiosis, (ii) natural variation in rhizobium partner quality is mediated in part by key symbiosis genes on the symbiotic plasmid, and (iii) differentiation at selected genes occurred in the context of otherwise recombining genomes, resembling eukaryotic models of adaptation.

SUBMITTER: Klinger CR

PROVIDER: S-EPMC4810848 | biostudies-literature | 2016 Mar

REPOSITORIES: biostudies-literature

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Project description:UnlabelledThe ability to reduce atmospheric nitrogen (N2) to ammonia, known as N2 fixation, is a widely distributed trait among prokaryotes that accounts for an essential input of new N to a multitude of environments. Nitrogenase reductase gene (nifH) composition suggests that putative N2-fixing heterotrophic organisms are widespread in marine bacterioplankton, but their autecology and ecological significance are unknown. Here, we report genomic and ecophysiology data in relation to N2 fixation by three environmentally relevant heterotrophic bacteria isolated from Baltic Sea surface water: Pseudomonas stutzeri strain BAL361 and Raoultella ornithinolytica strain BAL286, which are gammaproteobacteria, and Rhodopseudomonas palustris strain BAL398, an alphaproteobacterium. Genome sequencing revealed that all were metabolically versatile and that the gene clusters encoding the N2 fixation complex varied in length and complexity between isolates. All three isolates could sustain growth by N2 fixation in the absence of reactive N, and this fixation was stimulated by low concentrations of oxygen in all three organisms (≈ 4 to 40 µmol O2 liter(-1)). P. stutzeri BAL361 did, however, fix N at up to 165 µmol O2 liter(-1), presumably accommodated through aggregate formation. Glucose stimulated N2 fixation in general, and reactive N repressed N2 fixation, except that ammonium (NH4 (+)) stimulated N2 fixation in R. palustris BAL398, indicating the use of nitrogenase as an electron sink. The lack of correlations between nitrogenase reductase gene expression and ethylene (C2H4) production indicated tight posttranscriptional-level control. The N2 fixation rates obtained suggested that, given the right conditions, these heterotrophic diazotrophs could contribute significantly to in situ rates.ImportanceThe biological process of importing atmospheric N2 is of paramount importance in terrestrial and aquatic ecosystems. In the oceans, a diverse array of prokaryotes seemingly carry the genetic capacity to perform this process, but lack of knowledge about their autecology and the factors that constrain their N2 fixation hamper an understanding of their ecological importance in marine waters. The present study documents a high variability of genomic and ecophysiological properties related to N2 fixation in three heterotrophic isolates obtained from estuarine surface waters and shows that these organisms fix N2 under a surprisingly broad range of conditions and at significant rates. The observed intricate regulation of N2 fixation for the isolates indicates that indigenous populations of heterotrophic diazotrophs have discrete strategies to cope with environmental controls of N2 fixation. Hence, community-level generalizations about the regulation of N2 fixation in marine heterotrophic bacterioplankton may be problematic.

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Ecological genomics of mutualism decline in nitrogen-fixing bacteria.

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