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. 2025 Feb 21;11(8):eadt2147.
doi: 10.1126/sciadv.adt2147. Epub 2025 Feb 19.

The Rise of Algae promoted eukaryote predation in the Neoproterozoic benthos

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The Rise of Algae promoted eukaryote predation in the Neoproterozoic benthos

Daniel B Mills et al. Sci Adv. .

Abstract

The proliferation of marine algae in the Neoproterozoic Era is thought to have stimulated the ecology of predatory microbial eukaryotes. To test this proposal, we introduced algal particulate matter (APM) to marine sediments underlying a modern marine oxygen minimum zone with bottom-water oxygen concentrations approximating those of the late Neoproterozoic water column. We found that under anoxia, APM significantly stimulated microbial eukaryote gene expression, particularly genes involved in anaerobic energy metabolism and phagocytosis, and increased the relative abundance of 18S rRNA from known predatory clades. We additionally confirmed that APM promoted the reproduction of benthic foraminifera under anoxia with higher-than-expected net growth efficiencies. Overall, our findings suggest that algal biomass exported to the Neoproterozoic benthos stimulated the ecology of benthic predatory protists under anoxia, thereby creating more modern food webs by enhancing the transfer of fixed carbon and energy to eukaryotes occupying higher trophic levels, including the earliest benthic metazoans.

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Figures

Fig. 1.
Fig. 1.. The effect of added algal matter on eukaryote gene expression in anoxic sediment incubations.
(A) The percentage of expressed open reading frames (ORFs) across the domains of life as a function of both time and the presence of APM. Asterisks denote statistically significant differences (two-sided t test; P values < 0.05; n = 8). Error bars represent SD. By 7 and 10 days, O2 was below detection (fig. S1). (B) Significant overexpression of eukaryote genes in APM treatments (n = 5) relative to the controls (n = 5), with genes involved in phagocytosis labeled and marked in red. The vertical dashed line separates expressed genes that either increased or decreased in relative abundance with APM relative to the controls, while the horizontal dashed line represents the P value cutoff for determining statistical significance (two-sided t test; P values < 0.05). (C) Phylogenetic tree of 18S rRNA OTUs significantly (two-sided t test: P < 0.05; n = 10; fig. S5) overexpressed in the APM treatments, with bubbles proportional to the fold change in 18S rRNA expression between the treatments and controls. d, days; GTPases, guanosine triphosphatases.
Fig. 2.
Fig. 2.. Heatmap of expressed eukaryote genes involved in anaerobic energy metabolism and phagocytosis.
(A) Genes involved in anaerobic energy metabolism in eukaryotes [collected from (41)] from in situ water and sediment samples from the BUS (left side; n = 27), as well as experimental time points (right; n = 13). (B) Genes involved in phagocytosis (, –39, 94) across the same sampled metatranscriptomes. Heatmap coloring corresponds to the relative levels of gene expression (that is, percentage of total expressed genes), with darker colors indicating higher relative abundances. Blue and red squares at the bottom of the plot display the presence or absence of O2 (above or below 1 μM O2), respectively. NADH, reduced form of nicotinamide adenine dinucleotide; ATPases, adenosine triphosphatases; VAMP, vesicle-associated membrane protein; WASH, Wiskott–Aldrich syndrome protein and SCAR homologue.
Fig. 3.
Fig. 3.. Anaerobic growth and growth efficiencies of benthic foraminifera.
(A) Concentration of foraminifera cells (tests) of different genera in the APM treatments and controls compared to the in situ state (t0), according to four different size fractions. (B) Phylogenetic tree (PhyML) of foraminifera nirK transcripts, as well as a likely nirK expressed by Candidatus Azoamicus ciliaticola, a denitrifying endosymbiont of anaerobic ciliates (23). The panel to the right displays the expression of nirK ORFs in both the treatments and controls over time expressed as reads per kilobase mapped (RPKM). Note that the eukaryote nirK is only expressed in the presence of APM at 7 and 10 days under anoxia. (C) Net growth efficiency (NGE; see Materials and Methods) estimated for benthic foraminifera consuming 13C-labeled APM in the presence and absence of O2 and under three sets of assumptions regarding the fractional contribution of foraminifera to 13CO2 production from 13C-labeled APM. Error bars represent SE. Dashed lines represent calculated NGEs from (28) and (45). Note that the calculated NGEs for foraminifera growing under anoxia is higher than those calculated for fermenting (nonrespiring) protists under anoxia (28). h, hours. d, days.
Fig. 4.
Fig. 4.. The evolution of benthic food webs from the mid- to late-Proterozoic Eon.
(A) Simplified (nonexhaustive) schematic of the microbial loop before the primary acquisition of plastids yet after the origin of phagotrophy (the eukaryote feeding mode in which microbial prey are internalized via phagocytosis). Marine surface waters in equilibrium with the atmosphere at this time likely had O2 concentrations corresponding to 1 to 10% of modern atmospheric saturation and were therefore severely hypoxic (4.8 to 22 μM O2) by modern oceanographic standards (3). The earliest phagotrophs were probably (bacterivorous) protozoa that phagocytosed bacteria (and archaea) from both the water column and benthos, before the origin of eukaryote-on-eukaryote predation (eukaryovory) (95). (B) Simplified schematic of the microbial loop toward the end of the Proterozoic Eon, after the permanent establishment of abundant eukaryote primary producers. By this time, the O2 content of shallow marine environments was likely increasing but was still “hypoxic” (22 to 63 μM O2) by modern standards (3). The bold arrows indicate the consumption of exported APM by benthic eukaryovorous protozoa (as demonstrated by this study), followed by the consumption of these protozoa by the earliest benthic animals (metazoans). By the end-Proterozoic, metazoans likely consumed dissolved organic carbon (DOC) via osmotrophy (75, 96), mat-forming bacteria and associated protozoa via both surface grazing (77) and external digestion (78), planktonic microbes via suspension feeding (76), and benthic microbes via infaunal deposit feeding (76). Schematic inspired by figure 1 from (25).

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