Abstract
Diazotrophic cyanobacteria, those capable of fixing di-nitrogen (N2), are considered one of the major sources of new nitrogen (N) in the oligotrophic tropical ocean, but direct incorporation of diazotrophic N into food webs has not been fully examined. In the Amazon River-influenced western tropical North Atlantic (WTNA), diatom diazotroph associations (DDAs) and the filamentous colonial diazotrophs Trichodesmium have seasonally high abundances. We sampled epipelagic mesozooplankton in the Amazon River plume and WTNA in May–June 2010 to investigate direct grazing by mesozooplankton on two DDA populations: Richelia associated with Rhizosolenia diatoms (het-1) and Hemiaulus diatoms (het-2), and on Trichodesmium using highly specific qPCR assays targeting nitrogenase genes (nifH). Both DDAs and Trichodesmium occurred in zooplankton gut contents, with higher detection of het-2 predominantly in calanoid copepods (2.33–16.76 nifH copies organism-1). Abundance of Trichodesmium was low (2.21–4.03 nifH copies organism-1), but they were consistently detected at high salinity stations (>35) in calanoid copepods. This suggests direct grazing on DDAs, Trichodesmium filaments and colonies, or consumption as part of sinking aggregates, is common. In parallel with the qPCR approach, a next generation sequencing analysis of 16S rRNA genes identified that cyanobacterial assemblage associated with zooplankton guts was dominated by the non-diazotrophic unicellular phylotypes Synechococcus (56%) and Prochlorococcus (26%). However, in two separate calanoid copepod samples, two unicellular diazotrophs Candidatus Atelocyanobacterium thalassa (UCYN-A) and Crocosphaera watsonii (UCYN-B) were present, respectively, as a small component of cyanobacterial assemblages (<2%). This study represents the first evidence of consumption of DDAs, Trichodesmium, and unicellular cyanobacteria by calanoid copepods in an area of the WTNA known for high carbon export. These diazotroph populations are quantitatively important in the global N budget, widespread and hence, the next step is to accurately quantify grazing. Nonetheless, these results highlight a direct pathway of diazotrophic N into the food web and have important implications for biogeochemical cycles, particularly oligotrophic regions where N2 fixation is the main source of new nitrogen.
Highlights
Primary production in the marine environment is mostly limited by nitrogen availability (Gruber, 2008)
We note that for the 16S rRNA analysis we consider our results representative of the zooplankton “microbiome,” similar to other studies (Scavotto et al, 2015; Shoemaker and Moisander, 2015), we focus our results on the cyanobacteria and are confident that the cleaning methods adapted from Boling et al (2012) were adequate enough and our results represent the cyanobacteria consumed by the various mesozooplankton
In order to account for low gene copies due to gut degradation, we suggest future work include controlled grazing experiments using a culture of the targeted diazotroph for analyses so that a differential length amplification Quantitative PCR (qPCR) method, similar to that utilized in Troedsson et al (2009), could account for DNA degradation, and be used to estimate grazing rate on diazotrophs
Summary
Primary production in the marine environment is mostly limited by nitrogen availability (Gruber, 2008). In the open ocean dissolved inorganic nitrogen (DIN) is rare, diazotrophic organisms, those able to utilize N2 through the process of biological N2 fixation, play a significant role as drivers of primary production by provision of new nitrogen (N) (Dugdale and Goering, 1967). Diatom diazotroph associations (DDAs) are of considerable interest because they are capable of expansive blooms and high rates of N2 fixation (Carpenter et al, 1999; Foster et al, 2007; Subramaniam et al, 2008; Villareal et al, 2012). Blooms of DDAs are important for enhancing carbon export from surface waters (Cooley and Yager, 2006; Subramaniam et al, 2008; Karl et al, 2012; Yeung et al, 2012)
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