Abstract

Microbial nitrogen fixation (diazotrophy) is a functional trait widely associated with tropical reef-building (scleractinian) corals. While the integral role of nitrogen fixation in coral nutrient dynamics is recognized, its ecological significance across different coral functional groups remains yet to be evaluated. Here we set out to compare molecular and physiological patterns of diazotrophy (i.e., nifH gene abundance and expression as well as nitrogen fixation rates) in two coral families with contrasting trophic strategies: highly heterotrophic, free-living members of the family Fungiidae (Pleuractis granulosa, Ctenactis echinata), and mostly autotrophic coral holobionts with low heterotrophic capacity (Pocilloporidae: Pocillopora verrucosa, Stylophora pistillata). The Fungiidae exhibited low diazotroph abundance (based on nifH gene copy numbers) and activity (based on nifH gene expression and the absence of detectable nitrogen fixation rates). In contrast, the mostly autotrophic Pocilloporidae exhibited nifH gene copy numbers and gene expression two orders of magnitude higher than in the Fungiidae, which coincided with detectable nitrogen fixation activity. Based on these data, we suggest that nitrogen fixation compensates for the low heterotrophic nitrogen uptake in autotrophic corals. Consequently, the ecological importance of diazotrophy in coral holobionts may be determined by the trophic functional group of the host.

Highlights

  • Tropical reef-building corals are holobionts consisting of the coral animal host, dinoflagellate algae of the genus Symbiodinium, and a diverse assemblage of other microbes (Rohwer et al, 2002)

  • P. verrucosa and S. pistillata showed 23- and 431-fold higher relative diazotroph abundance and 95- to 480-fold higher relative gene expression compared to P. granulosa, respectively (Supplementary Table S1)

  • The present study investigated physiological and molecular patterns of nitrogen fixation along with diazotroph abundance in corals representing two different trophic functional groups

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Summary

Introduction

Tropical reef-building (scleractinian) corals are holobionts consisting of the coral animal host, dinoflagellate algae of the genus Symbiodinium, and a diverse assemblage of other microbes (Rohwer et al, 2002). These microbes form host-specific associations and provide key functional traits within the coral holobiont. Scleractinian coral holobionts are mixotrophic, i.e., can draw energy and nutrients from both autotrophic and heterotrophic sources. We set out to compare rates of nitrogen fixation with coral-associated diazotroph abundance and activity in a comparative coral taxonomic framework assaying highly heterotrophic (Pleuractis granulosa, Ctenactis echinata) and mostly autotrophic (Pocillopora verrucosa, Stylophora pistillata) corals (Muscatine et al, 1984; Muscatine and Kaplan, 1994; Houlbrèque and Ferrier-Pagès, 2009; Ziegler et al, 2014). We assessed coral tissue-associated relative gene copy numbers and expression of the nifH gene, a common biomarker for diazotrophs (Gaby and Buckley, 2012) using quantitative PCR (qPCR) to investigate relative diazotroph community sizes along with their activity

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