Recent observations of N 2 fixation rates (NFR) and the presence of nitrogenase (nifH) genes from heterotrophic N 2 -fixing (diazotrophic) prokaryotes in unusual habitats challenge the paradigm that pelagic marine N 2 fixation is constrained to cyanobacteria in warm, oligotrophic, surface waters. Here, we compare NFR and diazotrophic diversity (assessed via high-throughput nifH sequencing) from a region known to be dominated by cyanobacterial diazotrophs (the North Pacific Subtropical Gyre, NPSG) to two regions dominated by heterotrophic diazotrophs: the Eastern South Pacific (ESP, from the Chilean upwelling system to the subtropical gyre) and the Pacific Northwest coastal upwelling system (PNW). We observed distinct biogeographical patterns among the three regions. Diazotrophic community structure differed strongly between the NPSG, dominated by cyanobacterium UCYN-A, and the ESP, dominated by heterotrophic nifH group 1J/1K, yet surface NFR were similar in magnitude (up to 5.1 nmol N L 21 d 21). However, while diverse, predominantly heterotrophic nifH genes were recovered from the PNW and the mesopelagic of the NPSG, NFR were undetectable in both of these environments (although glucose amendments stimulated low rates in the deep NPSG). Our work suggests that while diazotrophs may be nearly omnipresent in marine waters, the activity of this functional group is regionally restricted. Further, we show that the detection limits of the 15 N 2 fixation assay suggest that many of the low NFR reported for the mesopelagic (often < 0.1 nmol N L 21 d 21 in the literature) are not indicative of active diazotrophy, highlighting the challenges of assessing the ecosystem significance of heterotrophic diazotrophs.
Dinitrogen (N 2 ) fixation is an important source of biologically reactive nitrogen (N) to the global ocean. The magnitude of this flux, however, remains uncertain, in part because N 2 fixation rates have been estimated following divergent protocols and because associated levels of uncertainty are seldom reported-confounding comparison and extrapolation of rate measurements. A growing number of reports of relatively low but potentially significant rates of N 2 fixation in regions such as oxygen minimum zones, the mesopelagic water column of the tropical and subtropical oceans, and polar waters further highlights the need for standardized methodological protocols for measurements of N 2 fixation rates and for calculations of detection limits and propagated error terms. To this end, we examine current protocols of the 15 N 2 tracer method used for estimating diazotrophic rates, present results of experiments testing the validity of specific practices, and describe established metrics for reporting detection limits. We put forth a set of recommendations for best practices to estimate N 2 fixation rates using 15 N 2 tracer, with the goal of fostering transparency in reporting sources of uncertainty in estimates, and to render N 2 fixation rate estimates intercomparable among studies.
Human land use alters soil microbial composition and function in a variety of systems, although few comparable studies have been done in tropical forests and tropical agricultural production areas. Logging and the expansion of oil palm agriculture are two of the most significant drivers of tropical deforestation, and the latter is most prevalent in Southeast Asia. The aim of this study was to compare soil fungal communities from three sites in Malaysia that represent three of the most dominant land-use types in the Southeast Asia tropics: a primary forest, a regenerating forest that had been selectively logged 50 years previously, and a 25-year-old oil palm plantation. Soil cores were collected from three replicate plots at each site, and fungal communities were sequenced using the Illumina platform. Extracellular enzyme assays were assessed as a proxy for soil microbial function. We found that fungal communities were distinct across all sites, although fungal composition in the regenerating forest was more similar to the primary forest than either forest community was to the oil palm site. Ectomycorrhizal fungi, which are important associates of the dominant Dipterocarpaceae tree family in this region, were compositionally distinct across forests, but were nearly absent from oil palm soils. Extracellular enzyme assays indicated that the soil ecosystem in oil palm plantations experienced altered nutrient cycling dynamics, but there were few differences between regenerating and primary forest soils. Together, these results show that logging and the replacement of primary forest with oil palm plantations alter fungal community and function, although forests regenerating from logging had more similarities with primary forests in terms of fungal composition and nutrient cycling potential. Since oil palm agriculture is currently the mostly rapidly expanding equatorial crop and logging is pervasive across tropical ecosystems, these findings may have broad applicability.
The number of marine environments known to harbor dinitrogen (N 2)-fixing (diazotrophic) microorganisms is increasing, prompting a reassessment of the biogeography of marine diazotrophs and N 2 fixation rates (NFRs). Here, we investigate the diversity, abundance, and activity of diazotrophic microorganisms in the North Pacific Subtropical Gyre (NPSG), a diazotrophic habitat, and the North Pacific Transition Zone (NPTZ), a region characterized by strong physical, chemical, and biological gradients. Samples were collected on two springtime meridional cruises during 2016 and 2017, spanning from 23.5 N to 41.4 N along 158 W. We observed an abrupt decrease in diazotrophic abundances near the southern edge of the NPTZ, which coincided with a salinity front and with a $10-fold increase in Synechococcus abundance, but without a concomitant change in phosphate or nitrate concentrations. In NPSG waters south of this diazotrophic boundary, nifH genes and NFRs were consistently detected and diazotrophic communities were dominated by UCYN-A, an uncultivated, symbiotic cyanobacterium (2.8 × 10 3 to 1.0 × 10 6 nifH gene copies L −1). There was a significant positive relationship between quantitative polymerase chain reaction-derived UCYN-A nifH gene abundances and community NFRs in the NPSG, suggesting a large contribution of UCYN-A to community NFRs. In the NPTZ waters to the north, NFRs were low or undetected and nifH genes were rare, with the few detected sequences represented by UCYN-A and noncyanobacterial diazotrophs. The patterns we observed in UCYN-A abundance in the context of local biogeochemistry suggest that the environmental controls of this organism may differ from those of cultivated marine cyanobacterial diazotrophs.
Filamentous diazotrophic Cyanobacteria of the genus Trichodesmium, often found in colonial form, provide an important source of new nitrogen to tropical and subtropical marine ecosystems. Colonies are composed of several clades of Trichodesmium in association with a diverse community of bacterial and eukaryotic epibionts. We used high-throughput 16S rRNA and nifH gene sequencing, carbon (C) and dinitrogen (N2) fixation assays, and metagenomics to describe the diversity and functional potential of the microbiome associated with Trichodesmium colonies collected from the North Pacific Subtropical Gyre (NPSG). The 16S rRNA and nifH gene sequences from hand-picked colonies were predominantly (>99%) from Trichodesmium Clade I (i.e., T. thiebautii), which is phylogenetically and ecologically distinct from the Clade III IMS101 isolate used in most laboratory studies. The bacterial epibiont communities were dominated by Bacteroidetes, Alphaproteobacteria, and Gammaproteobacteria, including several taxa with a known preference for surface attachment, and were relatively depleted in the unicellular Cyanobacteria and small photoheterotrophic bacteria that dominate NPSG surface waters. Sequencing the nifH gene (encoding a subcomponent of the nitrogenase enzyme) identified non-Trichodesmium diazotrophs that clustered predominantly among the Cluster III nifH sequence-types that includes putative anaerobic diazotrophs. Trichodesmium colonies may represent an important habitat for these Cluster III diazotrophs, which were relatively rare in the surrounding seawater. Sequence analyses of nifH gene transcripts revealed several cyanobacterial groups, including heterocystous Richelia, associated with the colonies. Both the 16S rRNA and nifH datasets indicated strong differences between Trichodesmium epibionts and picoplankton in the surrounding seawater, and also between the epibionts inhabiting Trichodesmium puff and tuft colony morphologies. Metagenomic and 16S rRNA gene sequence analyses suggested that lineages typically associated with a copiotrophic lifestyle comprised a large fraction of colony-associated epibionts, in contrast to the streamlined genomes typical of bacterioplankton in these oligotrophic waters. Additionally, epibiont metagenomes were enriched in specific genes involved in phosphate and iron acquisition and denitrification pathways relative to surface seawater metagenomes. We propose that the unique microbial consortium inhabiting colonies has a significant impact on the biogeochemical functioning of Trichodesmium colonies in pelagic environments.
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