Global phylogeography and microdiversity of the marine diazotrophic photoautotrophs Trichodesmium and UCYN-A

Abstract

Photoautotrophic diazotrophs, specifically the genera Trichodesmium and UCYN-A, play a pivotal role in marine nitrogen cycling through their capacity for nitrogen fixation. Despite their global distribution, the microdiversity and environmental drivers of these diazotrophs remain underexplored. This study provides a comprehensive analysis of the global diversity and distribution of Trichodesmium and UCYN-A using the nitrogenase gene (nifH) as a genetic marker. We sequenced 954 samples from the Pacific, Atlantic, and Indian Oceans as part of the Bio-GO-SHIP project. Our results reveal significant phylogenetic and biogeographic differences between and within the two genera. Trichodesmium exhibited greater microdiversity compared to UCYN-A, with clades showing region-specific distribution. Trichodesmium clades were primarily influenced by temperature and nutrient availability. They were particularly frequent in regions of phosphorus stress. In contrast, UCYN-A was most frequently observed in regions experiencing iron stress. UCYN-A clades demonstrated more homogeneous distributions, with a single sequence variant within the UCYN-A1 clade dominating across varied environments. The biogeographic patterns and environmental correlations of Trichodesmium and UCYN-A highlight the role of microdiversity in their ecological adaptation and reflect their different ecological strategies. These findings underscore the importance of characterizing the global patterns of fine-scale genetic diversity to better understand the functional roles and distribution of marine nitrogen-fixing photoautotrophs.IMPORTANCEThis study provides insights into the global diversity and distribution of nitrogen-fixing photoautotrophs, specifically Trichodesmium and UCYN-A. We sequenced 954 oceanic samples of the nifH nitrogenase gene and uncovered significant differences in microdiversity and environmental associations between these genera. Trichodesmium showed high levels of sequence diversity and region-specific clades influenced by temperature and nutrient availability. In contrast, UCYN-A exhibited a more uniform distribution, thriving in iron-stressed regions. Quantifying these fine-scale genetic variations enhances our knowledge of their ecological roles and adaptations, emphasizing the need to characterize the genetic diversity of marine nitrogen-fixing prokaryotes.

Keywords: cyanobacteria; environmental microbiology; marine microbiology; microbial ecology; nitrogen fixation; phylogeography.

Fig 1

Global distribution of samples. Map of sampling locations for nifH amplicon sequences. Samples are grouped and colored based on region, using warm colors for the Atlantic Ocean, blue and green for the Pacific Ocean, and purple for the Indian Ocean samples.

Fig 2

Phylogenetic tree of top 100 ASVs in Trichodesmium (A) and UCYN-A (B). Most abundant ASV for each clade is denoted by an *. Bootstrap values out of 100 are displayed at each node. ASV naming scheme is from most abundant to least abundant. Environmental counts of the top 25 ASV in Trichodesmium (C) and UCYN-A (D). Shannon diversity of Trichodesmium and UCYN-A (E). Mean value shown by red dot (Trichodesmium mean = 0.55 and UCYN-A mean = 0.30).

Fig 3

Biogeography of Trichodesmium and UCYN-A clades. Amplicon-derived relative abundance of Trichodesmium vs UCYNA-A (A). A value of 1 represents 100% Tricho, while a value of 0 represents 100% UCYN-A. Relative abundance of individual clades out of total Trichodesmium abundance (B–E). Relative abundance of individual clades out of total UCYN-A abundance (F–H).

Fig 4

PCoA of Trichodesmium and UCYN-A beta-diversity (A and B). Correlations between environmental measurements (black arrows, bold label) and clade relative abundance (gray arrows, non-bolded label) and PCoA components. Exact values can be found in Tables S1 and S2 (A and B). Spearman correlations on the relative abundance of Trichodesmium and UCYN-A (C), Trichodesmium clade relative abundance (D), and UCYN-A clade relative abundance (E). Correlations are made with the following environmental data: sea surface temperature (SST), nutricline depth (nutricline), phosphorus stress (Ω P), iron stress (Ω Fe), and nitrogen stress (Ω N).