Bacteriohopanetetrol-<i>x</i>: constraining its application as a lipid biomarker for marine anammox using the water column oxygen gradient of the Benguela upwelling system

Interpreting lipid biomarkers in the sediment archive requires a good understanding of their application and limitations in modern systems. Recently it was discovered that marine bacteria performing anaerobic ammonium oxidation (anammox), belonging to the genus Ca. Scalindua, uniquely synthesize a stereoisomer of bacteriohopanetetrol (“BHT-x”). The ratio of BHT-x over total bacteriohopanetetrol (BHT, ubiquitously synthesized by diverse bacteria) has been suggested as a proxy for water column anoxia. As BHT has been found in sediments over 50 Myr old, BHT-x has the potential to complement and extend the sedimentary biomarker record of marine anammox, conventionally constructed using ladderane lipids. Yet, little is known about the distribution of BHT-x in relation to the distribution of ladderanes and to the genetic evidence of Ca. Scalindua in modern marine systems. Here, we investigate the distribution of BHT-x and the application of the BHT-x ratio in relation to distributions of ladderane intact polar lipids (IPLs), ladderane fatty acids (FAs) and Ca. Scalindua 16S rRNA genes in suspended particulate matter (SPM) from the water column of the Benguela upwelling system (BUS), sampled across a large oxygen gradient. In BUS SPM, high BHT-x abundances were restricted to the oxygen-deficient zone on the continental shelf (at [O2] < 45 µmol L−1, in all but one case). High BHT-x abundances co-occurred with high abundances of the Ca. Scalindua 16S rRNA gene (relative to the total number of bacterial 16S rRNA genes) and ladderane IPLs. At shelf stations with [O2] > 50 µmol L−1, the BHT-x ratio was < 0.04 (in all but one case). In apparent contradiction, ladderane FAs and low abundances of BHT and BHT-x (resulting in BHT-x ratios > 0.04) were also detected in oxygenated offshore waters ([O2] up to 180 µmol L−1), whereas ladderane IPLs were undetected. The index of ladderane lipids with five cyclobutane rings (NL5) correlates with in situ temperature. NL5-derived temperatures suggested that ladderane FAs in the offshore waters were not synthesized in situ but were transported down-slope from warmer shelf waters. Thus, in sedimentary archives of systems with known lateral organic matter transport, such as the BUS, relative BHT and BHT-x abundances should be carefully considered. In such systems, a higher BHT-x ratio may act as a safer threshold for deoxygenation and/or Ca. Scalindua presence: our results and previous studies indicate that a BHT-x ratio of ≥ 0.2 is a robust threshold for oxygen-depleted waters ([O2] < 50 µmol kg−1). In our data, ratios of ≥ 0.2 coincided with Ca. Scalindua 16S rRNA genes in all samples (n=62), except one. Lastly, when investigating in situ anammox, we highlight the importance of using ladderane IPLs over BHT-x and/or ladderane FAs; these latter compounds are more recalcitrant and may derive from transported fossil anammox bacteria remnants.

Toward a Solution of the “Peruvian Puzzle”: Pelagic Food-Web Structure and Trophic Interactions in the Northern Humboldt Current Upwelling System Off Peru

The northern Humboldt Current upwelling system (HCS) belongs to the most productive marine ecosystems, providing five to eight times higher fisheries landings per unit area than other coastal upwelling systems. To solve this “Peruvian puzzle”, to elucidate the pelagic food-web structure and to better understand trophic interactions in the HCS, a combined stable isotope and fatty acid trophic biomarker approach was adopted for key zooplankton taxa and higher trophic positions with an extensive spatial coverage from 8.5 to 16°S and a vertical range down to 1,000 m depth. A pronounced regional shift by up to ∼5‰ in the δ15N baseline of the food web occurred from North to South. Besides regional shifts, δ15N ratios of particulate organic matter (POM) also tended to increase with depth, with differences of up to 3.8‰ between surface waters and the oxygen minimum zone. In consequence, suspension-feeding zooplankton permanently residing at depth had up to ∼6‰ higher δ15N signals than surface-living species or diel vertical migrants. The comprehensive data set covered over 20 zooplankton taxa and indicated that three crustacean species usually are key in the zooplankton community, i.e., the copepods Calanus chilensis at the surface and Eucalanus inermis in the pronounced OMZ and the krill Euphausia mucronata, resulting in an overall low number of major trophic pathways toward anchovies. In addition, the semi-pelagic squat lobster Pleuroncodes monodon appears to play a key role in the benthic-pelagic coupling, as indicated by highest δ13C’ ratios of −14.7‰. If feeding on benthic resources and by diel vertical migration, they provide a unique pathway for returning carbon and energy from the seafloor to the epipelagic layer, increasing the food supply for pelagic fish. Overall, these mechanisms result in a very efficient food chain, channeling energy toward higher trophic positions and partially explaining the “Peruvian puzzle” of enormous fish production in the HCS.

Bacteriohopanetetrol-x: constraining its application as a lipid biomarker for marine anammox using the water column oxygen gradient of the Benguela upwelling system

Interpreting lipid biomarkers in the sediment archive requires a good understanding of their application and limitations in modern systems. Recently it was discovered that marine bacteria performing anaerobic ammonium oxidation (anammox), belonging to the genus Ca. Scalindua, uniquely synthesize a stereoisomer of bacteriohopanetetrol (‘BHT-x’). The ratio of BHT-x over total bacteriohopanetetrol (BHT; ubiquitously synthesized by diverse bacteria) has been suggested as a proxy for water column anoxia. As BHT has been found in sediments over 50 Myr old, BHT-x has the potential to complement and extend the sedimentary biomarker record of marine anammox, conventionally constructed using ladderane lipids. Yet, little is known about the distribution of BHT-x in relation to the distribution of ladderanes and to the genetic evidence of Ca. Scalindua in modern marine systems. Here, we investigate the distribution of BHT-x and the application of the BHT-x ratio in relation to distributions of intact polar (IPL) ladderane lipids, ladderane fatty acids (FAs) and Ca. Scalindua 16S rRNA genes in suspended particulate matter (SPM) from the water column, sampled across a large oxygen gradient in the Benguela upwelling system (BUS). In BUS SPM, high BHT-x abundances were constrained to the oxygen deficient zone on the continental shelf (at [O2] < 45 µmol L−1, in all but one case). High BHT-x abundances co-occurred with high abundances of the Ca. Scalindua 16S rRNA gene (relative to the total number of bacterial 16S rRNA genes) and ladderane IPLs. At shelf stations with [O2] > 50 µmol L−1, the BHT-x ratio was < 0.04 (in all but one case). In apparent contradiction, ladderane FAs and low abundances of BHT and BHT-x (resulting in BHT-x ratio’s > 0.04) were also detected in oxygenated offshore waters ([O2] up to 180 µmol L−1), whereas ladderane IPLs were undetected. NL5-derived temperatures suggested that ladderane FAs in the offshore waters were not synthesized in situ but derived from warmer shelf waters. Thus, in sedimentary archives of systems with known lateral organic matter transport, such as the BUS, relative BHT and BHT-x abundances should be carefully considered. In such systems, a higher BHT-x ratio may act as a safer threshold for deoxygenation and/or Ca. Scalindua presence: in the BUS, at [O2] > 50 µmol L−1, the BHT-x ratio was < 0.18 at both off -and onshore sites (in all but one case) and a ratio > 0.18 corresponded in all cases (except one) with the presence of Ca. Scalindua 16S rRNA genes. Lastly, when investigating in situ anammox, we highlight the importance of using ladderane IPLs over BHT-x and/or ladderane FAs; these latter compounds are more recalcitrant and may derive from transported fossil anammox bacteria remnants.

Oxygen and Nutrient Trapping in the Southern Benguela Upwelling System

The Benguela Upwelling System in the southeast Atlantic Ocean is of crucial socio-economic importance due to its high productivity. However, predicting its response to global change and understanding past changes are still great challenges. Here, we compile data obtained from a research cruise and an oceanographic mooring to demonstrate that a topographically steered nutrient trapping zone develops in a narrow belt along the coast during the main upwelling season in austral spring and summer in the southern Benguela Upwelling System. High nutrient concentrations within this zone increase the impact of upwelling on the productivity of the southern Benguela Upwelling System, but the efficient nutrient trapping operates at the expense of decreasing oxygen concentrations. This enhances the probability of anoxic events emerging toward the end of the upwelling season. However, at the end of the upwelling season, the front that separates the coastally trapped waters from open shelf waters weakens or even collapses due to upwelling cessation and the reversing current regime. This, in addition to a stronger vertical mixing caused by winter cooling, fosters the ventilation of the nutrient trapping zone, which reestablishes during the following upwelling season. The postulated intensification of upwelling and changes in the ecosystem structure in response to global warming seem to reduce the nutrient trapping efficiency by increasing offshore advection of surface waters and plankton blooms. The intensified upwelling and resulting lower biological oxygen consumption appears to mask the expected impacts of global warming on the oxygen minimum zone (OMZ) in the southern Benguela Upwelling System. In contrast to other OMZs, including those in northern Benguela Upwelling Systems, the OMZ in the southern Benguela Upwelling System reveals so far no detectable long-term decrease in oxygen. Thus, the nutrient trapping efficiency seems to be a critical feature mitigating global change impacts on the southern Benguela Upwelling System. Since it is topographically steered, regional impacts on the nutrient trapping efficiency appear also to explain varying responses of upwelling systems to global change as the comparison between southern and northern Benguela Upwelling System shows. This emphasizes the need for further and more comparable studies in order to better understand the response of Eastern Boundary Upwelling Systems and their ecosystem services to global change.

Mixing and Phytoplankton Growth in an Upwelling System

Previous studies focused on understanding the role of physical drivers on phytoplankton bloom formation mainly used indirect estimates of turbulent mixing. Here we use weekly observations of microstructure turbulence, dissolved inorganic nutrients, chlorophyll a concentration and primary production carried out in the Ría de Vigo (NW Iberian upwelling system) between March 2017 and May 2018 to investigate the relationship between turbulent mixing and phytoplankton growth at different temporal scales. In order to interpret our results, we used the theoretical framework described by the Critical Turbulent Hypothesis (CTH). According to this conceptual model if turbulence is low enough, the depth of the layer where mixing is active can be shallower than the mixed-layer depth, and phytoplankton may receive enough light to bloom. Our results showed that the coupling between turbulent mixing and phytoplankton growth in this system occurs at seasonal, but also at shorter time scales. In agreement with the CTH, higher phytoplankton growth rates were observed when mixing was low during spring-summer transitional and upwelling periods, whereas low values were described during periods of high mixing (fall-winter transitional and downwelling). However, low mixing conditions were not enough to ensure phytoplankton growth, as low phytoplankton growth was also found under these circumstances. Wavelet spectral analysis revealed that turbulent mixing and phytoplankton growth were also related at shorter time scales. The higher coherence between both variables was found in spring-summer at the ~16–30 d period and in fall-winter at the ~16–90 d period. These results suggest that mixing could act as a control factor on phytoplankton growth over the seasonal cycle, and could be also involved in the formation of occasional short-lived phytoplankton blooms.