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.

Taxonomy of Middle Miocene foraminifera from the northern Namibian continental shelf

Middle Miocene foraminifera from the northern Namibian outer continental shelf are indicators of a period prior to the initiation of the Benguela Upwelling System (BUS). This study provides an update to the occurrence and taxonomy of Miocene foraminifera from the continental margin of Namibia. The taxonomy of 51 benthic and 12 planktic foraminiferal species from the northern Namibian shelf are discussed, their stratigraphic significance given, and their ecological preferences and regional distribution summarised within this study. The identification of extinct planktic foraminifera provided key stratigraphic control for the middle Miocene strata of this region. The taxa identified in this study provide a distinct and different assemblage to the overlying younger strata. Many of the species recorded in this study have not been identified in the region and are reported for the first time from the middle Miocene on the southwestern continental shelf of Africa, off Namibia. A total of 47 species are identified and discussed for the first time from this region. Nineteen species recorded in this study are extinct and eleven taxa reported here have previously only been reported on the genus level on the southwestern shelf of South Africa. Seven benthic species (Amphicoryna scalaris, Marginulina obesa, Glandulina laevigata, Globocassidulina subglobosa, Uvigerina peregrina, Sphaeroidina bulloides and Melonis affinis) and two planktic species (Globigerina bulloides and Orbulina universa) did not disappear from the regional stratigraphy and continued to occur in Plio-Pleistocene to Recent sediments along the southwestern continental shelf of Africa.

Giant sulfur bacteria (Beggiatoaceae) from sediments underlying the Benguela upwelling system host diverse microbiomes

Due to their lithotrophic metabolisms, morphological complexity and conspicuous appearance, members of the Beggiatoaceae have been extensively studied for more than 100 years. These bacteria are known to be primarily sulfur-oxidizing autotrophs that commonly occur in dense mats at redox interfaces. Their large size and the presence of a mucous sheath allows these cells to serve as sites of attachment for communities of other microorganisms. But little is known about their individual niche preferences and attached microbiomes, particularly in marine environments, due to a paucity of cultivars and their prevalence in habitats that are difficult to access and study. Therefore, in this study, we compare Beggiatoaceae strain composition, community composition, and geochemical profiles collected from sulfidic sediments at four marine stations off the coast of Namibia. To elucidate community members that were directly attached and enriched in both filamentous Beggiatoaceae, namely Ca. Marithioploca spp. and Ca. Maribeggiatoa spp., as well as non-filamentous Beggiatoaceae, Ca. Thiomargarita spp., the Beggiatoaceae were pooled by morphotype for community analysis. The Beggiatoaceae samples collected from a highly sulfidic site were enriched in strains of sulfur-oxidizing Campylobacterota, that may promote a more hospitable setting for the Beggiatoaceae, which are known to have a lower tolerance for high sulfide to oxygen ratios. We found just a few host-specific associations with the motile filamentous morphotypes. Conversely, we detected 123 host specific enrichments with non-motile chain forming Beggiatoaceae. Potential metabolisms of the enriched strains include fermentation of host sheath material, syntrophic exchange of H2 and acetate, inorganic sulfur metabolism, and nitrite oxidation. Surprisingly, we did not detect any enrichments of anaerobic ammonium oxidizing bacteria as previously suggested and postulate that less well-studied anaerobic ammonium oxidation pathways may be occurring instead.

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.

The relation of wind-driven coastal and offshore upwelling in the Benguela Upwelling System

Spatial and temporal variations of nutrient-rich upwelled water across the major eastern boundary upwelling systems are primarily controlled by the surface wind with different, and sometimes contrasting, impacts on coastal upwelling systems driven by alongshore wind and offshore upwelling systems driven by the local wind-stress-curl. Here, concurrently measured wind-fields, satellite-derived Chlorophyll-a concentration along with a state-of-the-art ocean model simulation spanning 2008-2018 are used to investigate the connection between coastal and offshore physical drivers of the Benguela Upwelling System (BUS). Our results indicate that the spatial structure of long-term mean upwelling derived from Ekman theory and the numerical model are fairly consistent across the entire BUS and closely followed by the Chlorophyll-a pattern. The variability of the upwelling from the Ekman theory is proportionally diminished with offshore distance, whereas different and sometimes opposite structures are revealed in the model-derived upwelling. Our result suggests the presence of sub-mesoscale activity (i.e., filaments and eddies) across the entire BUS with a large modulating effect on the wind-stress-curl-driven upwelling off Lüderitz and Walvis Bay. In Kunene and Cape Frio upwelling cells, located in the northern sector of the BUS, the coastal upwelling and open-ocean upwelling frequently alternate each other, whereas they are modulated by the annual cycle and mostly in phase off Walvis Bay. Such a phase relationship appears to be strongly seasonally dependent off Lüderitz and across the southern BUS. Thus, our findings suggest this relationship is far more complex than currently thought and seems to be sensitive to climate changes with short- and far-reaching consequences for this vulnerable marine ecosystem.

Carotenoid biomarkers in Namibian shelf sediments: Anoxygenic photosynthesis during sulfide eruptions in the Benguela Upwelling System

Aromatic carotenoid-derived hydrocarbon biomarkers are ubiquitous in ancient sediments and oils and are typically attributed to anoxygenic phototrophic green sulfur bacteria (GSB) and purple sulfur bacteria (PSB). These biomarkers serve as proxies for the environmental growth requirements of PSB and GSB, namely euxinic waters extending into the photic zone. Until now, prevailing models for environments supporting anoxygenic phototrophs include microbial mats, restricted basins and fjords with deep chemoclines, and meromictic lakes with shallow chemoclines. However, carotenoids have been reported in ancient open marine settings for which there currently are no known modern analogs that host GSB and PSB. The Benguela Upwelling System offshore Namibia, known for exceptionally high primary productivity, is prone to recurrent toxic gas eruptions whereupon hydrogen sulfide emanates from sediments into the overlying water column. These events, visible in satellite imagery as water masses clouded with elemental sulfur, suggest that the Benguela Upwelling System may be capable of supporting GSB and PSB. Here, we compare distributions of biomarkers in the free and sulfur-bound organic matter of Namibian shelf sediments. Numerous compounds—including acyclic isoprenoids, steranes, triterpanes, and carotenoids—were released from the polar lipid fractions upon Raney nickel desulfurization. The prevalence of isorenieratane and β-isorenieratane in sampling stations along the shelf verified anoxygenic photosynthesis by low-light-adapted, brown-colored GSB in this open marine setting. Renierapurpurane was also present in the sulfur-bound carotenoids and was typically accompanied by lower abundances of renieratane and β-renierapurpurane, thereby identifying cyanobacteria as an additional aromatic carotenoid source.