Ecology

BOOK REVIEW
24 January 2022

A call for governments to save soil

To ensure food security, the world must stop letting fertile soil wash and blow away.

Emma Marris

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Emma Marris

Emma Marris is an environmental writer who lives in Oregon.

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Rock becomes visible as topsoil is eroded away.Credit: Martin Harvey/Getty

A World Without Soil: The Past, Present, and Precarious Future of the Earth Beneath Our Feet Jo Handelsman Yale Univ. Press (2021)Soil creates life from death. The production of more than 95% of the food we eat relies on soil, a heady mix of rock particles, decaying organic matter, roots, fungi and microorganisms. Yet this precious resource is eroding at a global average of 13.5 tonnes per hectare per year. Instead of nourishing crops, fertile topsoil is ending up in inconvenient places such as ditches, reservoirs and the ocean.Microbiologist Jo Handelsman takes on the challenge of making readers care in A World Without Soil, aided by environmental researcher Kayla Cohen. Their prologue takes the form of a letter about soil erosion that Handelsman wishes she had sent to US president Barack Obama while working in the White House’s Office of Science and Technology Policy in the mid-2010s. Alas, she did not understand the true gravity of the problem until the waning days of the administration. Her biggest regret? That she wasn’t able to make soil management the federal priority she thinks it should be.Soil can be created over time, as dead things break down and contribute energy and nutrients to an ecosystem based on the underlying rock. But it erodes 10–30 times faster than it is produced. Globally, erosion reduces annual crop yields by 0.3%. At that rate, 10% of production could be lost by 2050. In erosion hotspots such as Nigeria, 80% of the land has been degraded. In Iowa, up to 17% of land is almost devoid of topsoil. Almost more convincing than the many facts and figures is a colour photograph of a field in Iowa with so little topsoil that the pale, lifeless sandy rubble beneath pokes through.Age-old solutionsA sense of dread builds in the chapters that cover the basic science of soil as well as the causes and consequences of its erosion. The last part of the book brings a burst of enthusiasm, as the authors turn to possible solutions — many of them simple, and some millennia old. These involve improving holding capacity through planting diverse crops in rotation; increasing organic content with additions such as compost and biochar; reducing the erosional effects of water and wind by reshaping the land with contouring, terraces, windbreaks and the like; and ploughing as little as possible.In a chapter on traditional soil-management techniques around the world, Handelsman and Cohen describe deep black “plaggen” soils on Scottish islands, made rich with cattle manure; rice terraces managed for 2,000 years by the Ifugao people in the Philippines; the milpa farming system of the Maya in Latin America, with its 25-year rotation of crops including trees; and compost made of seaweed, shells and plant material by the Māori in New Zealand. Each system yields rich agricultural productivity while maintaining deep banks of carbon-rich, fertile soil. “We know how to do this,” write Handelsman and Cohen.

Cactus farming in Mexico, where the traditional system of crop rotation helps to replenish the soil.Credit: Omar Torres/AFP/Getty

Why, then, is fertile soil being allowed to wash and blow away? The answer, not surprisingly, rests in the shackles of global capitalism. Farming’s profit margins are razor-thin, forcing producers to plant the highest-yielding variety of the highest-profit crop from field edge to field edge every season. Terracing, rotating crops and forgoing tilling enrich soil in the long run, but nibble into profits this year. And farmers can’t pay their mortgages or lease equipment with the aroma of deep black topsoil.
Food systems: seven priorities to end hunger and protect the planet
Handelsman and Cohen urge the world to demand real change in how mainstream agricultural production is managed. “The burden of protecting soil cannot be relegated to indigenous people and environmental activists,” they note. But their specific suggestions are a little underwhelming. They join the calls for international soil treaties, but given how poorly climate treaties have worked, I am cynical about the potential of such agreements. Countries seem likely to both under-promise and under-deliver unless there are costly penalties for failure. The same goes for the consumer-facing labels that the authors propose for food produced on farms that are working to improve their soil. Similar labels have not put a meaningful dent in climate change or other environmental problems — and many customers cannot afford to spend more on “soil-friendly” food.Top-down changeWhat farming needs is a top-down overhaul. Handelsman and Cohen gesture at this with proposed discounts on crop-insurance premiums for farmers who increase the carbon in their soil. More is needed. Governments must pay farmers to build soil. In the United States, farmers can apply for funding for anti-erosion improvements through the Environmental Quality Incentives Program, run by the Department of Agriculture. Funding announced this month will increase the amount of land planted with cover crops to 12 million hectares by 2030 — but even that would represent only some 7% of US cropland. It is not enough.We need to change how we think of farming. We have already begun to move towards a model in which farmers are less independent businesspeople growing and selling food, and more government-supported land stewards managing a complex mix of food production, soil fertility, wildlife habitat and more. Around the world, many farmers depend on subsidies, drought relief and payments from piecemeal schemes to conserve soil and nature. Such programmes — currently small-scale, ad hoc fixes for a broken system — should be the core of the agricultural sector.Our land, our fresh water, our biodiversity and our soil are too precious to be destroyed by the market price of commodity grains and other foodstuffs. We must invest deeply and thoughtfully in our farmers so that they can invest deeply and thoughtfully in the land, becoming holistic landscape-management professionals. This is the future of farming.

Nature 601, 503-504 (2022)
doi: https://doi.org/10.1038/d41586-022-00158-8

Competing Interests
The author declares no competing interests.

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Our results show that differences in environmental conditions between inland and coastal sinkholes, caused mainly by the inflow of seawater in the latter, influence the microbial community structure of their sediments. Furthermore, the microbial community structure also varied within the sinkholes and according to the sediment zone sampled, suggesting that a connection between the atmosphere in the outermost location of the sediments and sunlight creates an environment distinct from that found in deeper caves. Together with the different environmental factors that were measured (in situ physicochemical composition of water and sediment) these characteristics could drive niche-specific microbial community structures associated with the sediment zones. Additionally, beta-diversity analysis showed separate clustering of the sediment microbial communities from the coastal and inland sinkholes, and of the WM zone from cavern and cave zones at both sinkholes. Microbial community structure associated with karst environments have shown to be significantly influenced by environmental factors as seen in the Bahamian blue holes19, a coastal sinkhole13, a Floridan anchialine sinkhole20, and sediments from Chinese karst caves21.Microbial communities from karst sediments can be limited by nutrients such as carbon, phosphorus, and nitrogen21, therefore, influencing their structure. Differences in the microbial community composition associated with multiple environmental factors (moisture, type of niche, nitrogen) were also reported in karst cave sediments from China21. Previous studies had shown there was no effect on the alpha diversity of water column assemblages in the Yucatan groundwater associated with the type of sinkhole (inland or coastal)6. However, this observation may be limited due to the low sample number used in the study6. For other karst sinkholes, the microbial community dynamics differ between the water column and the sediments6,22,23,24.The karst caves and sinkholes of the underground river in Yucatan are characterized by low phosphorus concentrations and high levels of nitrate, mostly related to Anthropocentric activities (urban developments, farms and agriculture)3. The inland sinkhole at Noh Mozón showed the highest concentration of nitrate detected in the study and, not surprisingly, the area is surrounded by agricultural fields. The presence of organic matter in the sinkholes from the Yucatan peninsula are highly dependent on the connection between the cave systems, on the levels of exposure to light, and on their morphology3. High concentrations of organic carbon (661 ± 132 μM) and methane (6466 ± 659 nM) have been reported in the top layer of the water masses in coastal sinkholes before13. In this study, the highest concentration of organic carbon was observed in the sediments from the coastal sinkhole, likely originating from the surrounding vegetation and from seawater intrusion. We hypothesize that the differences in nutrients found at these two types of sinkholes influence the structure of their microbial communities.Other environmental factors such as pH and dissolved oxygen (DO), may also contribute significantly to the composition and structure of microbial communities, as seen in freshwater lake sediments22. Davis and Garey20 reported distinct microbial communities with unique functions for each water layer from an anchialine sinkhole from the Florida karst aquifer and suggested that this occurred as a result of the influence of the hydrochemistry, including differences in the concentration carbon and other nutrients from the environment20. Analyses of the sinkhole caves from the Yucatan underwater river support observations that physical and chemical parameters create distinct ecological niches which host unique microbes, as a high abundance of exclusive (not shared) ASVs were observed in the three sediment zones at both locations.The taxonomic diversity from the coastal and inland sinkholes included Chloroflexi, Crenarchaeota, Desulfobacterota, Proteobacteria, Nitrospirota, Bacteroidota, and Firmicutes as the most abundant phyla in the sediment samples, however, there were differences in the relative abundance associated with the type of sinkhole and sediment zone. Some of these phyla (Chloroflexi, Proteobacteria, and Bacteroidetes) have been reported in sediments from freshwater karst sinkholes from Lake Huron25 in water and sediments from other sinkholes in the Yucatan peninsula6, and in the karst caves bacteriome from southwest China21. A study that included coastal marine sediments from two sites in the Yucatan peninsula, showed high abundances of Spirochaeta, Desulfococcus, Clostridium, Psychrobacter26, four genera that were abundant in the coastal sinkhole. However, Desulfococcus, Synechococcus were also abundant in the inland sinkhole. Of the most abundant genera reported for sediments from different marine environments in the Yucatan coast23, Acinetobacter, Desulfotignum, Desulfovibrio, Pseudomonas, Sedimenticola, and Sulfurimonas were also present in the coastal sinkhole while only Pseudomonas and Sedimenticola were also present in the inland sinkhole23. The high number of families shared between the coastal sinkhole and marine sediments from the Yucatan coast, together with the salinity levels registered at the bottom layer of the water column in the coastal sinkhole, suggest an interconnection between these two environments which shapes the microbial communities present in the sediments of caverns and caves of this sinkhole. The genus Nitrospira was abundant in the WM from the coastal sinkhole and in all sediment zones from the inland sinkhole. This genus has been reported as one of the most abundant in the surface of speleothems from El Zapote coastal sinkhole2, and is considered a complete ammonia oxidizer (comammox), meaning it converts ammonia to nitrate through nitrite. A negative correlation between abundance of this genus and salinity has been reported before, which could explain the low concentration of Nitrospira in the cavern and cave from the coastal sinkhole, where the highest salinity was observed27. Connectivity between coastal sinkholes and the ocean, as well as the terrestrial input of soil organic matter (OM) has been reported for the underground karst aquifer in the Yucatan peninsula13. As in other sediments, degradation of OM is carried out by several MFGs including acetogenic bacteria, methanogens, and sulfate reducers13,20,28. When these MFGs were analyzed in coastal and inland sinkholes, differences in their relative abundances were clearly marked by the type of sinkhole and by the sediment zone analyzed, supporting the hypothesis that environmental differences drive microbial community distributions in these niches. The high abundance of sulfate-reducing bacteria (SRB) in the three sediment zones from the coastal sinkhole suggests that sulfate reduction is a predominant function. SRB degrade organic matter using sulfate with sulfide as waste or end-product19,30, originating hydrogen sulfide (H2S)29, which could explain the low concentration of sulfate the hydrogen sulfide (H2S) cloud observed and previously reported in the WM zone of El Zapote coastal sinkhole30. In this study, high levels of sulfate (SO−4) were measured in the water samples from the cavern and cave zones from El Zapote sinkhole, which could be associated with sulfate-rich deposits, such as gypsum beds, which have been reported in other sinkholes from the Yucatan peninsula (up to 2400 mg/L of sulfate concentration)3. However, we do not disregard other possible sources of sulfate, associated with seawater intrusion or as a product of sulfide or sulfur oxidation29,31 by sulfur-oxidizing bacteria detected in this study.The inland sinkhole had a low concentration of sulfate and low abundances of SRB. The high abundance of methanogenic bacteria in the WM zone from the coastal sinkhole detected in the MFG analysis supports the previous hypothesis of acetoclastic methanogenesis due to high inputs of organic matter13. Methylotrophic bacteria were most abundant at the inland sinkhole in the WM zone, suggesting the presence of methyl compounds, such as methane or methanol which can be used as a source of carbon and energy32. High methane concentrations have been quantified in shallow water masses from the Yucatan aquifer system13, consistent with observations from this study. ‘Candidatus Methylomirabilis’ was identified in the sediment of the WM zone from Noh-Mozón and has been previously described as being able to perform nitrite-dependent anaerobic methane oxidation, using methane as electron donor and nitrate and nitrite as electron acceptors33, which would be possible in these sediments considering the low levels of oxygen (average of 2.3 mg/L) detected in the water column above them and assuming this would lead to lower levels of oxygen in the sediments. We hypothesize that bacteria from this genus could be using the nitrite produced by ammonia oxidizing bacteria and archaea observed in this zone (Nitrosomonadaceae, Nitrospiraceae, and Nitrosococcaceae). The low abundance of methanotrophic microbes in the coastal sinkhole (mainly the cavern and cave zones) could be derived from the high concentrations of hydrogen sulfide previously reported at this location, which have been suggested to be toxic to methane-oxidizing microbes34. Therefore, a decrease in the anaerobic oxidation of methane, and a poor methane removal capacity is hypothesized in the sediments from this coastal sinkhole. Further research could focus on the influence of the saline intrusion on methanotrophic microbes and methane levels in El Zapote sinkhole sediments. As expected, photosynthetic bacterial abundances differed with the type of sinkhole and sediment zone. Both sinkholes are so the presence of daylight can start the photosynthetic process which would occur most in the WM zone. However, only the inland sinkhole showed a high abundance of photosynthetic bacteria within its WM zone. The coastal sinkhole water column and sediments would be deprived of photosynthetic bacteria since the water source is the underground aquifer, lacks photosynthesizers. Ammonia oxidizing bacteria (AOB) and archaea (AOA), and nitrite-oxidizing bacteria (NOB) were relatively abundant in the three sediment zones from the inland sinkhole and in the WM from the coastal sinkhole, these observation at the WM from El Zapote agree with previous observations2. Anaerobic ammonium oxidation (anammox) uses nitrite (as a product of nitrate reduction), as electron acceptor35. The high levels of nitrate concentration in the water column from the three sediment zones at the inland sinkhole and at the WM from the coastal sinkhole may influence the abundance of AOB, AOA and NOB in the sediments from these zones, while NH4+ and nitrite values were below detection limit ( More

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Relationships between microbial diversity and base flow indexThe number of reads obtained per sample and total number of OTUs obtained after rarefaction for each gene dataset are summarised in Table S2. According to taxonomic analyses of our 16S rRNA gene dataset, archaeal communities in our river sediment samples consisted largely of OTUs assigned to the Woesarchaeota (20.8% of OTUs and 24.7% of reads) and Methanomicrobia (16.9% of OTUs and 31.8% of reads). Of the functional groups analysed here, ten OTUs were assigned to AOA, Nitrososphaera (n = 8) and Nitrosopumilus (n = 2), that together formed 4.8% of all archaeal 16S rRNA reads. A total of 137 OTUs were assigned to orders of methanogenic archaea, with 15.3% and 16% of archaeal reads assigned to the orders Methanomicrobiales and Methanosarcinales, respectively, with other methanogen orders constituting a further 6.7% of reads.Bacterial communities were more diverse and OTUs assigned to taxa within the functional groups analysed here formed a relatively small proportion of our bacterial 16S rRNA gene dataset. Ammonia oxidising bacteria were represented by only five OTUs (all assigned to Nitrosospira) that together constituted 0.02% of the total bacterial community across our sediments. A further 84 OTUs were assigned to methanotrophic genera, and these OTUs contributed a total of 0.88% of all bacterial 16S rRNA sequences. These were Methylobacter (30 OTUs, 0.7% of bacterial sequences), Methylophilus (15 OTUs, 0.1% of bacterial sequences), Methylosoma (7 OTUs, 0.004% of bacterial sequences), Methylomonas and Methylotenera (6 OTUs each, 0.02 and 0.002% of bacterial sequences, respectively), and Methylosarcina (5 OTUs, 0.002% of bacterial sequences), with a further eight genera represented by a total of 15 OTUs. As reported previously, no OTUs were assigned to known anammox genera, which were likely below the limit of detection in our study [8].The OTU richness of archaeal communities (based on 16S rRNA amplicons) was negatively, albeit weakly, related to BFI (coef = 0.52, z = −2.95, adj-D2 = 0.12, P  More