Abstract

Heterocystous cyanobacteria of biocrusts are key players for biological fixation in drylands, where nitrogen is only second to water as a limiting resource. We studied the niche partitioning among the three most common biocrust heterocystous cyanobacteria sts using enrichment cultivation and the determination of growth responses to temperature in 30 representative isolates. Isolates of Scytonema spp. were most thermotolerant, typically growing up to 40 °C, whereas only those of Tolypothrix spp. grew at 4 °C. Nostoc spp. strains responded well at intermediate temperatures. We could trace the heat sensitivity in Nostoc spp. and Tolypothrix spp. to N2-fixation itself, because the upper temperature for growth increased under nitrogen replete conditions. This may involve an inability to develop heterocysts (specialized N2-fixing cells) at high temperatures. We then used a meta-analysis of biocrust molecular surveys spanning four continents to test the relevance of this apparent niche partitioning in nature. Indeed, the geographic distribution of the three types was clearly constrained by the mean local temperature, particularly during the growth season. This allows us to predict a potential shift in dominance in many locales as a result of global warming, to the benefit of Scytonema spp. populations.

Highlights

  • In drylands, where plant growth is limited by water and nutrients, the soil surface can be occupied by communities of microorganisms known as biological soil crusts, which play crucial roles for the fertility and stability of drylands

  • Thermophysiological studies using laboratory isolates [31,32,33] or geographical distribution in molecular tallies [34] have shown that the three main clades of biocrust heterocystous cyanobacteria are characterized by different temperature ranges for growth: the Scytonema spp. clade tends to be more thermotolerant, whereas the Tolypothrix spp. clade shows psychrophilic preferences, and strains in the Nostoc spp. clade shows a preference for mild temperatures (15 to 30 ◦C)

  • Niloasrttooc tshpapt.fsoturanidnsinocncounp-hieedteornoclyystthoeums fielsaicmpeanrttouofs tchyeanteombapcetreartiauroef rsaonilgcer.uTshtsis[3n4i]c,haensdeparaltlieolns tihs esimmuilcahr mtootrheact ofnouspnidcuionunsonni-chheetedrioffceyrsetnoutisatfiiolanmoefnctyoaunsocbyaacnteorbiacktenroiawonffsroiml chruotstssp[r3in4]g,saantdtepmarpaellrealtsutrhees much more conspicuous niche differentiation of cyanobacteria known from hot springs at temperatures between 45-73 °C [67]

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Summary

Introduction

In drylands, where plant growth is limited by water and nutrients, the soil surface can be occupied by communities of microorganisms known as biological soil crusts (biocrusts; see [1] for a primer, and [2] for a monograph), which play crucial roles for the fertility and stability of drylands. Thermophysiological studies using laboratory isolates [31,32,33] or geographical distribution in molecular tallies [34] have shown that the three main clades of biocrust heterocystous cyanobacteria are characterized by different temperature ranges for growth: the Scytonema spp. clade tends to be more thermotolerant, whereas the Tolypothrix spp. clade shows psychrophilic preferences, and strains in the Nostoc spp. clade shows a preference for mild temperatures (15 to 30 ◦C) These results come from the evaluation of a restricted number of sites or strains, and the patterns were not always robust. Our results show that these cyanobacteria show markedly different thermophysiological patterns in culture and consistent world-wide distributions in nature This points to a potential for differential sensitivity among them to global warming, allowing us to predict a microbial replacement that biocrusts will have to contend with in future climate change scenarios

Enrichment Cultures
Experimental Organisms and Growth Conditions
Delineation of Temperature Range for Growth and Survival of Isolates
Influence of Diazotrophy on the Upper Temperature Limit for Growth
Heterocyst and Vegetative Cell Counts
Chlorophyll a Determination
Meta-analysis of Temperature Niches
Encrichment Cultivation
Heterocyst Frequency
Findings
Discussion
Full Text
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