N2 fixation, and the relative contribution of fixed N, in corals from Curaçao and Hawaii
Corals from Hawaii (Montipora capitata) and the Caribbean (brown and orange morphs of Montastraea cavernosa) have previously been shown to harbor symbiotic bacteria capable of fixing nitrogen (N2). Using a nitrogen tracer approach, we find that the rates of net photosynthesis and N2 fixation in M. capitata were significantly lower, while steady-state quantum yields of photosystem II (PSII) fluorescence (∆Fv/Fm′) were significantly higher, when compared to both color morphs of M. cavernosa where there was an inverse relationship between rates of photosynthesis and N2 fixation. However, the amount of fixed N contributing to Symbiodiniaceae N demand was consistent with their observed rates of N2 fixation. The lowest values occurred in M. capitata (0.034% ± 0.002 SE), and the brown morph of M. cavernosa had significantly lower values (1.081% ± 0.12 SE) compared to the orange morph (8.141% ± 0.36 SE). Additionally, for both the Symbiodiniaceae and microbial communities there were significant differences between species/color morphs where M. capitata was significantly different from both color morphs of M. cavernosa which were not significantly different from each other. An analysis of predicted metabolic activity, using PICRUSt2, also showed that the corals in this study were not predicted to be differentially enriched in genes involved in carbon metabolism, but genes involved in denitrification were predicted to be significantly enriched in both M. cavernosa orange and brown morphs. Genes involved in N2 fixation were, surprisingly, predicted to be enriched in M. cavernosa brown morphs. We suggest that the inhibition of nitrogenase by hyperoxia is one factor contributing to the low rates of N2 fixation in both M. capitata and M. cavernosa brown morphs.
KeywordsCoral Diazotrophs Microbiome Nitrogen fixation Symbiodiniaceae
Coral collection in Curaçao was assisted by Elizabeth Kintzing and Abbey Tedford. The coral collections in Curaçao were made under research permit (#2012/48584) issued by the Curaçao Ministry of Health, Environment and Nature (GMN) to the CARMABI foundation. At HIMB, coral collections were permitted under Division of Aquatic Resources Special Activity Permit No. 2015-17. The National Science Foundation (OCE 1437054 to MPL) supported this research.
MPL and KMM designed and conducted the collections and experiments. MPL analyzed all physiological and environmental data. KMM conducted all molecular processing and sequencing. MSP conducted all bioinformatics, statistical and PICRUSt2 analyses on sequence data. MPL, KMM and MSP wrote and approved the content of the manuscript.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
- Ainsworth TD, Krause L, Bridge T, Torda G, Raina JB, Zakrzewski M, Gates RD, Padilla-Gamiño JL, Spalding HL, Smith C, Woolsey ES, Boourne DG, Bongaerts P, Hoegh-Guldberg O, Leggatt W (2015) The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts. ISME J 9:2261–2274CrossRefGoogle Scholar
- Lahti L, Shetty S, Blake T, Salojarvi J (2017) Tools for microbiome analysis in R. Version 1.9.1. https://microbiome.github.io/tutorials/
- McFall-Ngai M, Hadfield MG, Bosch TCG, Carey HV, Domazet-Lošo T, Douglas AE, Dubilier N, Eberl G, Fukami T, Gilbert SF, Hentschel U, King N, Kjelleberg S, Knoll AH, Kremer N, Mazmanian SK, Metcalf JL, Nealson K, Pierce NE, Rawls JF, Reid A, Ruby EG, Rumpho M, Sanders JG, Tautz D, Wernegreen JJ (2013) Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci 110:3229–3236CrossRefGoogle Scholar
- Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, Minchin OR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2019) vegan: Community Ecology Package. R package version 2.4-3. https://CRAN.R-project.org/package=vegan