High Diazotrophic Diversity but Low N2 Fixation Activity in the Northern Benguela Upwelling System Confirming the Enigma of Nitrogen Fixation in Oxygen Minimum Zone Waters

Abstract

Oxygen minimum zones (OMZs) have been suggested as a suitable niche for the oxygen-sensitive process of biological fixation of dinitrogen (N2) gas. However, most N2 fixation rates reported from such waters are low. This low N2 fixation activity has been proposed to result from the unusual community of N2 fixers, in which cyanobacteria were typically underrepresented. The Northern Benguela Upwelling System (North BUS) is part of one of the most productive marine ecosystems and hosts a well-developed OMZ. Although previous observations indicated low to absent N2 fixation rates, the community composition of diazotrophs needed to understand the North BUS has not been described. Here, we present a first detailed analysis of the diazotrophic diversity in the North BUS OMZ and the Angola tropical zone (ATZ), based on genetic data and isotope speciation. Consistent with a previous study, we detected a slight N deficit in the OMZ, but isotope data did not indicate any active or past N2 fixation. The diazotroph community in the North BUS was dominated by non-cyanobacterial microbes clustering with members of gamma-proteobacteria, as is typical for other OMZ regions. However, we found a strikingly high diversity of Cluster III diazotrophs not yet described in other OMZs. In contrast to previous observations, we could also identify cyanobacteria of the clades Trichodesmium sp., UCYN-A and Cyanothece sp., in surface waters connected to or above the OMZ, which were potentially active as shown by the presence of genes and transcripts of the key functional marker gene for N2 fixation, nifH. While the detection of diazotrophs and the absence of active N2 fixation (based on isotopic speciation) are consistent with other OMZ observations, the detected regional variation in the diversity and presence of cyanobacteria indicate that we still are far from understanding the role of diazotrophs in OMZs, which, however, is relevant for understanding the N cycle in OMZ waters, as well for predicting the future development of OMZ biogeochemistry in a changing ocean.

Hydrodynamic regimes modulate nitrogen fixation and the mode of diazotrophy in Lake Tanganyika

“…The observed physical-biological coupling in Lake Tanganyika, a model system with respect to its hydrodynamics, may help to explain why N 2 fixation rates are generally low (<5 nM d −1 ) in some marine upwelling regions 15 , 22 , 26 – 28 , 30 , 80 , 81 . Many of these upwelling systems are also associated with gammaproteobacterial heterotrophic and often chemotactic diazotrophs 79 , like Pseudomonas 24 , 31 , 35 , 80 , 82 .…”

“…The observed physical-biological coupling in Lake Tanganyika, a model system with respect to its hydrodynamics, may help to explain why N 2 fixation rates are generally low (<5 nM d −1 ) in some marine upwelling regions 15 , 22 , 26 – 28 , 30 , 80 , 81 . Many of these upwelling systems are also associated with gammaproteobacterial heterotrophic and often chemotactic diazotrophs 79 , like Pseudomonas 24 , 31 , 35 , 80 , 82 . Moreover, when highly stratified conditions develop in marine upwelling regions (e.g., coastal sulfidic event 83 ), niches for phototrophic green sulfur bacteria become favorable 84 , consistent with observations in Lake Tanganyika’s Northern basin (Table 1 ).…”

Mineral-Bound Trace Metals as Cofactors for Anaerobic Biological Nitrogen Fixation

“…Under Mo-depleted conditions, the alternative nitrogenases were thought to fix N 2 . ,, However, the co-expression of all three nitrogenases occurs under conditions of various metal availability, and only a few studies provide evidence for the significant contribution of alternative nitrogenases. ,, The distribution of Mo-based metabolic processes in hot springs was not necessarily dependent on the soluble Mo concentration . The link between trace metal concentrations and nitrogenase activity is not always straightforward. , Therefore, there may be other controls on nitrogenase activity. − …”

Distribution of the N2‐fixing cyanobacterium Candidatus Atelocyanobacterium thalassa in the Mexican Pacific upwelling system under two contrasting El Niño Southern Oscillation conditions

“…Furthermore, the high nitrate (NO 3 − ) concentration often present in ODZs may not inhibit the growth of the UCYN‐A/haptophyte symbiosis, which can fix N 2 in NO 3 − ‐rich waters (Mills et al, 2020 ), an ability also observed in Crocosphaera watsonii (UCYN‐B) (Dekaezemacker & Bonnet, 2011 ; Großkopf & LaRoche, 2012 ). To date, UCYN‐B and non‐cyanobacterial diazotrophs have been found in oxygen‐deficient waters (Bonnet et al, 2013 ; Fernandez et al, 2011 ; Jayakumar et al, 2017 ; Jayakumar & Ward, 2020 ; Loescher et al, 2014 ; Löscher et al, 2020 ), whereas UCYN‐A has been detected in the Eastern Tropical North Pacific (ETNP), the Eastern Tropical South Pacific (ETSP) and the Northern Benguela Upwelling system, but only within their oxygenated waters (Reeder et al, 2022 ; Turk‐Kubo et al, 2014 , 2021 ; White et al, 2013 ). Little is known about the ecology of UCYN‐A in ODZs, therefore, providing information on its distribution in these oceanic regions is of utmost importance for a better understanding of the players involved in N fixation in ODZs.…”