Multicellularity is a key evolutionary innovation, leading to coordinated activity and resource sharing among cells, which generally occurs via the physical exchange of chemical compounds. However, filamentous cable bacteria display a unique metabolism in which redox transformations in distant cells are coupled via long-distance electron transport rather than an exchange of chemicals. This challenges our understanding of organismal functioning, as the link among electron transfer, metabolism, energy conservation, and filament growth in cable bacteria remains enigmatic. Here, we show that cells within individual filaments of cable bacteria display a remarkable dichotomy in biosynthesis that coincides with redox zonation. Nanoscale secondary ion mass spectrometry combined with ¹³C (bicarbonate and propionate) and ¹⁵N-ammonia isotope labeling reveals that cells performing sulfide oxidation in deeper anoxic horizons have a high assimilation rate, whereas cells performing oxygen reduction in the oxic zone show very little or no label uptake. Accordingly, oxygen reduction appears to merely function as a mechanism to quickly dispense of electrons with little to no energy conservation, while biosynthesis and growth are restricted to sulfide-respiring cells. Still, cells can immediately switch roles when redox conditions change, and show no differentiation, which suggests that the “community service” performed by the cells in the oxic zone is only temporary. Overall, our data reveal a division of labor and electrical cooperation among cells that has not been seen previously in multicellular organisms.

Due to decreases in seawater pH resulting from ocean acidification, permeable calcium carbonate reef sands are predicted to be net dissolving by 2050. However, the rate of dissolution and factors that control this rate remain poorly understood. Experiments performed in benthic chambers predict that reefs will become net dissolving when the aragonite saturation state (Ω_a) in sea water falls below ∼3, as underlying reef sediments start net dissolution due to lower saturation states in the pore water. We used flow-through reactors to investigate the rate of dissolution at various Ω_a at the pore scale. The sediment became net dissolving at Ω_a = 1.68–2.25, which is significantly greater than 1. This indicates that the bulk pore water does not represent conditions at the site of dissolution, and dissolution probably occurs in microniches inside porous sand grains. Measured dissolution rates were much higher under oxic conditions than anoxic conditions, but were not affected by the addition of carbonic anhydrase. Analysis of δ¹³C-CO₂ produced in the flow-through reactors revealed a bias in the conventional alkalinity anomaly method under anoxic conditions, showing that some of the CO₂ attributed to metabolism by may actually be derived from carbonate dissolution. This deviation likely originates from alkalinity consumption by fermentation, which masks the alkalinity generated by dissolution. Therefore, dissolution rates determined by alkalinity changes in reef sands with anaerobic metabolisms may underestimate actual values.

Cable bacteria are an emerging class of electroactive organisms that sustain unprecedented long-range electron transport across centimeter-scale distances. The local pathways of the electrical currents in these filamentous microorganisms remain unresolved. Here, the electrical circuitry in a single cable bacterium is visualized with nanoscopic resolution using conductive atomic force microscopy. Combined with perturbation experiments, it is demonstrated that electrical currents are conveyed through a parallel network of conductive fibers embedded in the cell envelope, which are electrically interconnected between adjacent cells. This structural organization provides a fail-safe electrical network for long-distance electron transport in these filamentous microorganisms. The observed electrical circuit architecture is unique in biology and can inspire future technological applications in bioelectronics.

Iron, manganese, and trace elements play an important role in the marine carbon cycle as they are limiting nutrients for marine primary productivity. Water column concentrations of these bio-essential elements are controlled by the balance between input and removal, with burial in marine sediments being the main sink. The efficiency of this burial sink is dependent on the redox state of the water column, with sediments underlying a sulphidic (euxinic) water column being the most efficient sinks for Fe, but also Mn and trace elements (Co, Cd, Ni, Mo, As, W, V, and U). Transient changes in ocean redox state can hence affect trace element burial, and correspondingly, the ocean's trace element inventory, but the impact of transient oxygenation events on trace element cycling is currently not well understood. Here, we investigate the impact of a natural oxygenation event on trace element release and burial in sediments of the Eastern Gotland Basin (EGB), a sub-basin of the Baltic Sea. After being anoxic (<0.5 µM O₂) for ∼10 years, the deep waters of the EGB experienced a natural oxygenation event (Major Baltic Inflow, MBI) in 2015. Following this oxygenation event, we deployed benthic chamber landers along a depth transect in the EGB in April 2016, 2017 and 2018. We complemented these in situ flux measurements with analyses of water column, solid phase and pore water chemistry. Overall, the event increased the benthic effluxes of dissolved trace elements, though particular responses were element-specific and were caused by different mechanisms. Enhanced fluxes of Cd and U were caused by oxidative remobilisation, while Ni showed little response to the inflow of oxygen. In contrast, enhanced release of Co, Mo, As, W, and V was caused by the enhanced transient input of Mn oxides into the sediment, whereas Fe oxides were of minor importance. Following the dissolution of the oxides in the sediment, Mn and W were nearly completely recycled back to the water column, while fractions of Fe, Co, Mo, As, and V were retained in the sediment. Our results suggest that transient oxygenation events in euxinic basins may decrease the water column inventory of certain trace elements (Fe, Co, Mo, As, and V), thus potentially affecting global marine primary productivity on longer timescales.

Filamentous cable bacteria exhibit long-range electron transport over centimetre-scale distances, which takes place in a parallel fibre structure with high electrical conductivity. Still, the underlying electron transport mechanism remains undisclosed. Here we determine the intrinsic electrical properties of the conductive fibres in cable bacteria from a material science perspective. Impedance spectroscopy provides an equivalent electrical circuit model, which demonstrates that dry cable bacteria filaments function as resistive biological wires. Temperature-dependent electrical characterization reveals that the conductivity can be described with an Arrhenius-type relation over a broad temperature range (− 195 °C to + 50 °C), demonstrating that charge transport is thermally activated with a low activation energy of 40–50 meV. Furthermore, when cable bacterium filaments are utilized as the channel in a field-effect transistor, they show n-type transport suggesting that electrons are the charge carriers. Electron mobility values are ~ 0.1 cm²/Vs at room temperature and display a similar Arrhenius temperature dependence as conductivity. Overall, our results demonstrate that the intrinsic electrical properties of the conductive fibres in cable bacteria are comparable to synthetic organic semiconductor materials, and so they offer promising perspectives for both fundamental studies of biological electron transport as well as applications in microbial electrochemical technologies and bioelectronics.

Cable bacteria represent a newly discovered group of filamentous microorganisms, which are capable of spatially separating the oxidative and reductive half-reactions of their sulfide-oxidizing metabolisms over centimeter distances. We investigated three ways that cable bacteria might interact with the nitrogen (N) cycle: (1) by reducing nitrate through denitrification or dissimilatory nitrate reduction to ammonium (DNRA) within their cathodic cells; (2) by nitrifying ammonium within their anodic cells; and (3) by indirectly affecting denitrification and/or DNRA by changing the Fe ²⁺ concentration in the surrounding sediment. We performed ¹⁵ N labeling laboratory experiments to measure these three processes using cable bacteria containing sediments from the Yarra River, Australia, and from Vilhelmsborg Sø, Denmark. Our results revealed that in the targeted systems, cable bacteria themselves did not perform significant rates of denitrification, DNRA, or nitrification. However, cable bacteria exhibited an important indirect effect, whereby they increased the Fe ²⁺ pool through iron sulfide dissolution. This elevated availability of Fe ²⁺ significantly increased DNRA and in some cases decreased denitrification. Thus, cable bacteria presence may affect the relative importance of DNRA in sediments and thus the extent by which bioavailable nitrogen is lost from the system.

Oxygen depletion in coastal waters may lead to release of toxic sulfide from sediments. Cable bacteria can limit sulfide release by promoting iron oxide formation in sediments. Currently, it is unknown how widespread this phenomenon is. Here, we assess the abundance, activity, and biogeochemical impact of cable bacteria at 12 Baltic Sea sites. Cable bacteria were mostly absent in sediments overlain by anoxic and sulfidic bottom waters, emphasizing their dependence on oxygen or nitrate as electron acceptors. At sites that were temporarily reoxygenated, cable bacterial densities were low. At seasonally hypoxic sites, cable bacterial densities correlated linearly with the supply of sulfide. The highest densities were observed at Gulf of Finland sites with high rates of sulfate reduction. Microelectrode profiles of sulfide, oxygen, and pH indicated low or no in situ cable bacteria activity at all sites. Reactivation occurred within 5 days upon incubation of an intact sediment core from the Gulf of Finland with aerated overlying water. We found no relationship between cable bacterial densities and macrofaunal abundances, salinity, or sediment organic carbon. Our geochemical data suggest that cable bacteria promote conversion of iron monosulfides to iron oxides in the Gulf of Finland in spring, possibly explaining why bottom waters in this highly eutrophic region rarely contain sulfide in summer.

The intestinal epithelium plays an essential role in the balance between tolerant and protective immune responses to infectious agents. In vitro models do not typically consider the innate immune response and gut microbiome in detail, so these models do not fully mimic the physiologic aspects of the small intestine. We developed and characterized a long-term in vitro model containing enterocyte, goblet, and immune-like cells exposed to a synthetic microbial community representative of commensal inhabitants of the small intestine. This model showed differential responses toward a synthetic microbial community of commensal bacterial inhabitants of the small intestine in the absence or presence of LPS from Escherichia coli 0111:B4. Simultaneous exposure to LPS and microbiota induced impaired epithelial barrier function; increased production of IL-8, IL-6, TNF-α, and C-X-C motif chemokine ligand 16; and augmented differentiation and adhesion of macrophage-like cells and the overexpression of dual oxidase 2 and TLR-2 and -4 mRNA. In addition, the model demonstrated the ability to assess the adhesion of specific bacterial strains from the synthetic microbial community—more specifically, Veillonella parvula—to the simulated epithelium. This novel in vitro model may assist in overcoming sampling and retrieval difficulties when studying host-microbiome interactions in the small intestine.—Calatayud, M., Dezutter, O., Hernandez-Sanabria, E., Hidalgo-Martinez, S., Meysman, F. J. R., Van de Wiele, T. Development of a host-microbiome model of the small intestine. FASEB J. 33, 3985–3996 (2019). www.fasebj.org.

Cable bacteria are multicellular, filamentous microorganisms that are capable of transporting electrons over centimeter-scale distances. Although recently discovered, these bacteria appear to be widely present in the seafloor, and when active they exert a strong imprint on the local geochemistry. In particular, their electrogenic metabolism induces unusually strong pH excursions in aquatic sediments, which induces considerable mineral dissolution, and subsequent mineral reprecipitation. However, at present, it is unknown whether and how cable bacteria play an active or direct role in the mineral reprecipitation process. To this end we present an explorative study of the formation of sedimentary minerals in and near filamentous cable bacteria using a combined approach of electron microscopy and spectroscopic techniques. Our observations reveal the formation of polyphosphate granules within the cells and two different types of biomineral formation directly associated with multicellular filaments of these cable bacteria: (i) the attachment and incorporation of clay particles in a coating surrounding the bacteria and (ii) encrustation of the cell envelope by iron minerals. These findings suggest a complex interaction between cable bacteria and the surrounding sediment matrix, and a substantial imprint of the electrogenic metabolism on mineral diagenesis and sedimentary biogeochemical cycling. In particular, the encrustation process leaves many open questions for further research. For example, we hypothesize that the complete encrustation of filaments might create a diffusion barrier and negatively impact the metabolism of the cable bacteria.

Biological electron transport is classically thought to occur over nanometre distances, yet recent studies suggest that electrical currents can run along centimetre-long cable bacteria. The phenomenon remains elusive, however, as currents have not been directly measured, nor have the conductive structures been identified. Here we demonstrate that cable bacteria conduct electrons over centimetre distances via highly conductive fibres embedded in the cell envelope. Direct electrode measurements reveal nanoampere currents in intact filaments up to 10.1 mm long (>2000 adjacent cells). A network of parallel periplasmic fibres displays a high conductivity (up to 79 S cm-1), explaining currents measured through intact filaments. Conductance rapidly declines upon exposure to air, but remains stable under vacuum, demonstrating that charge transfer is electronic rather than ionic. Our finding of a biological structure that efficiently guides electrical currents over long distances greatly expands the paradigm of biological charge transport and could enable new bio-electronic applications.

Climate variability has major implications for marine geochemical cycles and biogenic carbonate production. Therefore, past climate-driven changes in marine environments are often inferred from geochemical data of the marine carbonate archive. Proxy calibration studies are essential for the reconstruction of such past environmental changes. Here, we use the geochemical composition of living specimens of the benthic foraminifer Ammonia tepida at three sites in a seasonally hypoxic (oxygen concentration < 63 μmol/L) marine coastal system (Lake Grevelingen, the Netherlands) to explore the use of Mn/Ca as a proxy for coastal hypoxia. The study is based on samples from three stations along a depth transect, that show contrasts in the seasonal cycle of Mn ²⁺ concentrations in the pore water of the surface sediment. In general, the sediment and pore water geochemistry of the three stations in Lake Grevelingen show increased Mn ²⁺ concentrations in late winter/spring, combined with increased Mn refluxing in summer, which are due to cable bacteria activity and bottom water hypoxia/anoxia, respectively. Laser Ablation-ICP-MS (LA-ICP-MS) allowed a comparison of Mn/Ca ratios of different parts of the benthic foraminiferal test. Our results show that higher Mn/Ca ratios are registered at the deepest station, which experiences the longest and most severe seasonal periods of hypoxia/anoxia. Additionally, the signal preserved in the central part of the benthic foraminiferal tests, which is thought to reflect the entire calcification history of the analysed specimen, appears to be driven by high pore water Mn ²⁺ concentrations due to cable bacteria activity in late winter/spring. Conversely, high Mn/Ca ratios in the last chambers reflect increased Mn refluxing in the surface sediment due to summer hypoxia/anoxia. Thus, Mn/Ca ratios of A. tepida give insight into the complex spatial and temporal variability of pore water manganese.

Undigestible, insoluble food particles, such as wheat bran, are important dietary constituents that serve as a fermentation substrate for the human gut microbiota. The first step in wheat bran fermentation involves the poorly studied solubilization of fibers from the complex insoluble wheat bran structure. Attachment of bacteria has been suggested to promote the efficient hydrolysis of insoluble substrates, but the mechanisms and drivers of this microbial attachment and colonization, as well as subsequent fermentation remain to be elucidated. We have previously shown that an individually dependent subset of gut bacteria is able to colonize the wheat bran residue. Here, we isolated these bran-attached microorganisms, which can then be used to gain mechanistic insights in future pure culture experiments. Four healthy fecal donors were screened to account for inter-individual differences in gut microbiota composition. A combination of a direct plating and enrichment method resulted in the isolation of a phylogenetically diverse set of species, belonging to the Bacteroidetes, Firmicutes, Proteobacteria and Actinobacteria phyla. A comparison with 16S rRNA gene sequences that were found enriched on wheat bran particles in previous studies, however, showed that the isolates do not yet cover the entire diversity of wheat-bran colonizing species, comprising among others a broad range of Prevotella, Bacteroides and Clostridium cluster XIVa species. We, therefore, suggest several modifications to the experiment set-up to further expand the array of isolated species.

Coastal lagoon sediments are important for the biogeochemical carbon cycle at the land-ocean transition, as they form hotspots for organic carbon burial, as well as potential sites for authigenic carbonate formation. Here, we employ an early diagenetic model to quantify the coupled redox cycling of carbon, iron and sulphur in the sediments of the shallow Ghar El Melh (GEM) lagoon (Tunisia). The model simulated depth profiles show a good correspondence with available pore water data (dissolved inorganic carbon, NH ₄ ⁺ , total alkalinity, Ca ²⁺ , Fe ²⁺ and SO ₄ ²⁻ ) and solid phase data (organic matter, pyrite, calcium carbonate and iron (oxyhydr)oxides). This indicates that the model is able to capture the dominant processes influencing the sedimentary biogeochemical cycling. Our results show that sediment of the GEM lagoon is an efficient reactor for organic matter breakdown (burial efficiency < 10%), with an important role for aerobic respiration (32%) and sulphate reduction (61%). Despite high rates of sulphate reduction, free sulphide does not accumulate in the pore water, due to a large terrestrial input of reactive iron oxides and the efficient sequestration of free sulphide into iron sulphide phases. High pyrite burial (2.2 mmol FeS ₂ m ⁻² d ⁻¹ ) prevents the reoxidation of reduced sulphide, thus resulting in a low total oxygen uptake (4.7 mmol m ⁻² d ⁻¹ ) of the sediment and a relatively high oxygen penetration depth. The formation of pyrite also generates high amounts of alkalinity in the pore water, which stimulates authigenic carbonate precipitation (2.7 mmol m ⁻² d ⁻¹ ) and leads to alkalinity release to the overlying water (3.4 mmol m ⁻² d ⁻¹ ). Model simulations with and without an N-cycle reveal a limited influence of nitrification and denitrification on overall organic matter diagenesis. Overall, our study highlights the potential role of coastal lagoons for the global carbon and sulphur cycle, and their possible contribution to shelf alkalinity, which increases the buffering capacity of the coastal ocean for CO ₂ uptake.

Cable bacteria of the family Desulfobulbaceae form centimeter-long filaments comprising thousands of cells. They occur worldwide in the surface of aquatic sediments, where they connect sulfide oxidation with oxygen or nitrate reduction via long-distance electron transport. In the absence of pure cultures, we used single-filament genomics and metagenomics to retrieve draft genomes of 3 marine Candidatus Electrothrix and 1 freshwater Ca. Electronema species. These genomes contain >50% unknown genes but still share their core genomic makeup with sulfate-reducing and sulfur-disproportionating Desulfobulbaceae, with few core genes lost and 212 unique genes (from 197 gene families) conserved among cable bacteria. Last common ancestor analysis indicates gene divergence and lateral gene transfer as equally important origins of these unique genes. With support from metaproteomics of a Ca. Electronema enrichment, the genomes suggest that cable bacteria oxidize sulfide by reversing the canonical sulfate reduction pathway and fix CO₂ using the Wood–Ljungdahl pathway. Cable bacteria show limited organotrophic potential, may assimilate smaller organic acids and alcohols, fix N₂, and synthesize polyphosphates and polyglucose as storage compounds; several of these traits were confirmed by cell-level experimental analyses. We propose a model for electron flow from sulfide to oxygen that involves periplasmic cytochromes, yet-unidentified conductive periplasmic fibers, and periplasmic oxygen reduction. This model proposes that an active cable bacterium gains energy in the anodic, sulfide-oxidizing cells, whereas cells in the oxic zone flare off electrons through intense cathodic oxygen respiration without energy conservation; this peculiar form of multicellularity seems unparalleled in the microbial world.

Anoxic mineralization of organic matter releases dissolved inorganic carbon and produces reduced mineralization products. The reoxidation of these reduced compounds is essential for biogeochemical cycling in sediments and is mainly performed by chemoautotrophic microbes, which synthesize new organic carbon by dark CO₂ fixation. At present however, the biogeochemical importance of chemoautotrophy in high-latitude sediments is largely unknown. Here, we determine the seasonal variation in sedimentary chemoautotrophic production in Kobbefjord (SW Greenland). Intact sediment cores from the fjord were incubated, and dark CO₂ fixation was quantified by combining bacterial phospholipid-derived fatty acid analysis with ¹³C stable isotope probing (PLFA-SIP). Our results reveal a distinct seasonal cycle in chemoautotrophic activity, which increases after the spring bloom and shows lowest activity in the late winter when the fjord is covered by sea ice. The depth distribution of chemoautotrophic activity also varied seasonally, likely due to seasonal variation in the bioturbation activity of sediment infauna. Although chemoautotrophy rates (0.4 ± 0.2 mmol C m⁻² d⁻¹) were in the low range for coastal sediments, they are comparable to those from intertidal sandflats and brackish tropical lagoons, and scale with the sulfide production through sulfate reduction in the fjord. Chemoautotrophic production in these fjord sediments thus appears to be mainly driven by sulfide oxidation and can re-fix 4% of the CO₂ produced by mineralization.

Recently, a new group of multicellular microorganisms was discovered, called 'cable bacteria', which are capable of generating and mediating electrical currents across centimetre-scale distances. By transporting electrons from cell to cell, cable bacteria can harvest electron donors and electron acceptors that are widely separated in space, thus providing them with a competitive advantage for survival in aquatic sediments. The underlying process of long-distance electron transport challenges some long-held ideas about the energy metabolism of multicellular organisms and entails a whole new type of electrical cooperation between cells. This review summarizes the current knowledge about these intriguing multicellular bacteria. Cable bacteria are a newly discovered group of multicellular bacteria that generate and mediate electrical currents along their long filamentous body.Long-distance electron transport by cable bacteria bridges centimeter distances and extends the known length scale of biological electron transport by orders of magnitude.Long-distance electron transport allows cable bacteria to harvest electron donors and electron acceptors in widely separated locations, thus challenging long-held ideas on redox zonation in subsurface environments.By generating electrical currents, cable bacteria induce measurable electrical fields and potentials within their environment, and turn aquatic sediments into a living battery.Their widespread occurrence and strong imprint on local biogeochemistry suggests that cable bacteria are important in the cycling of carbon, sulfur, and other elements.

The biogeochemical cycle of iron is intricately linked to numerous element cycles. Although biological processes that catalyze the reductive side of the iron cycle are established, little is known about microbial oxidative processes on iron cycling in sedimentary environments—resulting in the formation of iron oxides. Here we show that a potential source of sedimentary iron oxides originates from the metabolic activity of iron-oxidizing bacteria from the class Zetaproteobacteria, presumably enhanced by burrowing animals in coastal sediments. Zetaproteobacteria were estimated to be a global total of 10²⁶ cells in coastal, bioturbated sediments, and predicted to annually produce 8 × 10¹⁵ g of Fe in sedimentary iron oxides—55 times larger than the annual flux of iron oxides deposited by rivers. These data suggest that iron-oxidizing Zetaproteobacteria are keystone organisms in marine sedimentary environments—despite their low numerical abundance—yet exert a disproportionate impact via the rejuvenation of iron oxides.

Electron transport within living cells is essential for energy conservation in all respiring and photosynthetic organisms. While a few bacteria transport electrons over micrometer distances to their surroundings, filaments of cable bacteria are hypothesized to conduct electric currents over centimeter distances. We used resonance Raman microscopy to analyze cytochrome redox states in living cable bacteria. Cable-bacteria filaments were placed in microscope chambers with sulfide as electron source and oxygen as electron sink at opposite ends. Along individual filaments a gradient in cytochrome redox potential was detected, which immediately broke down upon removal of oxygen or laser cutting of the filaments. Without access to oxygen, a rapid shift toward more reduced cytochromes was observed, as electrons were no longer drained from the filament but accumulated in the cellular cytochromes. These results provide direct evidence for long-distance electron transport in living multicellular bacteria.

Petroleum hydrocarbons reach the deep-sea following natural and anthropogenic factors. The process by which they enter deep-sea microbial food webs and impact the biogeochemical cycling of carbon and other elements is unclear. Hydrostatic pressure (HP) is a distinctive parameter of the deep sea, although rarely investigated. Whether HP alone affects the assembly and activity of oil-degrading communities remains to be resolved. Here we have demonstrated that hydrocarbon degradation in deep-sea microbial communities is lower at native HP (10 MPa, about 1000 m below sea surface level) than at ambient pressure. In long-term enrichments, increased HP selectively inhibited obligate hydrocarbon-degraders and downregulated the expression of beta-oxidation-related proteins (i.e., the main hydrocarbon-degradation pathway) resulting in low cell growth and CO₂ production. Short-term experiments with HP-adapted synthetic communities confirmed this data, revealing a HP-dependent accumulation of citrate and dihydroxyacetone. Citrate accumulation suggests rates of aerobic oxidation of fatty acids in the TCA cycle were reduced. Dihydroxyacetone is connected to citrate through glycerol metabolism and glycolysis, both upregulated with increased HP. High degradation rates by obligate hydrocarbon-degraders may thus be unfavourable at increased HP, explaining their selective suppression. Through lab-scale cultivation, the present study is the first to highlight a link between impaired cell metabolism and microbial community assembly in hydrocarbon degradation at high HP. Overall, this data indicate that hydrocarbons fate differs substantially in surface waters as compared to deep-sea environments, with in situ low temperature and limited nutrients availability expected to further prolong hydrocarbons persistence at deep sea.

The evolution of burrowing animals forms a defining event in the history of the Earth. It has been hypothesised that the expansion of seafloor burrowing during the Palaeozoic altered the biogeochemistry of the oceans and atmosphere. However, whilst potential impacts of bioturbation on the individual phosphorus, oxygen and sulphur cycles have been considered, combined effects have not been investigated, leading to major uncertainty over the timing and magnitude of the Earth system response to the evolution of bioturbation. Here we integrate the evolution of bioturbation into the COPSE model of global biogeochemical cycling, and compare quantitative model predictions to multiple geochemical proxies. Our results suggest that the advent of shallow burrowing in the early Cambrian contributed to a global low-oxygen state, which prevailed for ~100 million years. This impact of bioturbation on global biogeochemistry likely affected animal evolution through expanded ocean anoxia, high atmospheric CO₂ levels and global warming.