Genomics of variation in nitrogen fixation activity in a population of the thermophilic cyanobacterium Mastigocladus laminosus

Abstract

Variation in phenotypic traits that contribute to fitness influences a population's evolutionary response and its impact on ecosystem function following environmental change, yet its amount and nature are rarely known. Here, we investigated variation in nitrogen (N) fixation activity and its genetic basis for a random sample of laboratory strains of the cyanobacterium Mastigocladus laminosus from a N-limited, geothermally influenced stream in Yellowstone National Park. In a linear mixedeffects model, temperature and genetic differences among strains were the most important factors explaining variation in activity. Genome-wide analyses of genetic divergence between groups of strains that varied in N fixation activity revealed that few loci were strongly associated with these phenotypic differences. Notably, a single nonsynonymous polymorphism in the sulfate assimilation gene apsK explained 425% of the variation in activity at high temperature. We further identified a role for allelic variation of multiple terminal cytochrome oxidases for different aspects of N fixation. In addition, genomes of strains that fixed the most N overall contained a nonsense mutation in a histidine kinase gene that is expected to disrupt normal protein function and may result in transcriptional rewiring. This study illustrates how taking complementary approaches to link phenotype and genotype can inform our understanding of microbial population diversity.

Microbial Nitrogen Cycling in Antarctic Soils

“…Most of the surveys of N-cycling functional markers in Antarctic soils (summarised in Figure 1 ) have focused on the core genes involved in N-fixation ( nifH ), nitrification ( amoA ) and denitrification processes ( narG for nitrate reduction, nirK and nirS for nitrite reduction, norB for nitric oxide reduction and nosZ for nitrous oxide reduction). Shotgun metagenomic and amplicon sequencing approaches have been used to explore the presence/absence and diversity of key nitrogen cycling genes [ 72 , 73 ], while gene abundances have been monitored using qPCR and its variations [ 25 , 42 , 74 , 75 , 76 ] and Geochip microarray technologies [ 34 , 68 , 77 ].…”

Cyanobacteria and Alphaproteobacteria May Facilitate Cooperative Interactions in Niche Communities

“…In the zone below translucent rocks, referred to as the hypolithon, photoautotrophic, bacteria-dominated communities have crucial roles in biogeochemical processes by driving primary productivity ( Friedmann and Ocampo, 1976 ) and biomass production ( Chan et al, 2012 ). Photoautotrophs, such as Cyanobacteria, also contribute to soil carbon sequestration in deserts ( Cockell and Stokes, 2004 ) while heterocystous species directly fix atmospheric nitrogen ( Hutchins and Miller, 2017 ). There is direct evidence that these producers also mediate the transfer of nutrients and energy to heterotrophic bacteria ( Tracy et al, 2010 ; Cowan et al, 2011 ).…”

Evolutionary dynamics and structural consequences of de novo beneficial mutations and mutant lineages arising in a constant environment

“…Populations descending from such an ancestor carry an increased mutational load, but also have a built-in mechanism to lighten that load, specifically suppressing the burden of nonsense mutations that would otherwise result in loss-of-function (LOF). Laboratory evolution studies support the notion that LOF mutations can help drive adaptation [25,[114][115][116]. After all, metabolic networks can be reconfigured more easily by abolishing existing function(s) than by evolving altogether new ones [115]; thus, nonsense mutations or deletions sometimes confer greater fitness benefit than missense mutations affecting the same gene [116].…”