Interactions of the Microbial Iron and Methane Cycles in the Tundra Ecosystem

Award Number 1754358

This project was the most comprehensive analysis to date of the role of microbes that utilize iron as an energy source in the Arctic tundra play in permafrost underlain habitats on Alaska’s North Slope. These iron-cycling microbes can either capture enough energy to fix carbon dioxide and grow by oxidizing soluble ferrous iron to ferric iron, and produce rust-like precipitates of iron oxide, or, in the absence of oxygen, utilize the iron oxides to respire using organic matter or inorganic sources like hydrogen, and in this process reduce the insoluble minerals back to soluble ferrous iron. We conjecture that because the tundra regions of the North Slope are mineral soils underlain with continuous permafrost the entire hydrologic cycle is constrained to an active layer of approximately a half meter in summer. This provides an important, nearly continuous source of iron (the fourth most abundant element in Earth’s crust) that allows these iron-cycling microbes to flourish in moist wetland tundra habitats during an abbreviated growing season from mid-June to early September. Key discoveries from this work include:

• Documenting the extensiveness of these iron-rich habitats in wet-sedge meadows, stream banks, and small ponds, and characterizing the microbial communities as being unique to these habitats, and including diagnostic taxa known to either oxidize or reduce iron, but that these community structures are relatively conserved between the different habitat types.

• Developing a remote sensing algorithm that can used with drone-based, or other aerial imagery to document the presence of ‘iron mats’ associated with iron cycling microbes across the landscape. This will allow researchers to better document the extensiveness of these biologically driven iron-cycling processed across the tundra landscape using aerial imagery.

• Demonstrating that the iron oxides precipitated in these areas of active iron cycling sequester phosphorus, an important limiting nutrient in Arctic streams and rivers, thus indicating the iron cycle plays an important role in controlling phosphorus availability, and overall ecosystem function.

• Showing that anthropogenically disturbed tundra habitat can drastically alter and reduce iron cycling and that these altered sites do not show signs of biogeochemical recovery after 50 years.

• Observing that potent greenhouse gas methane is produced in these iron-rich wetland habitats, but that the extensive iron mat microbial communities are rich in microbes that utilize methane as an energy source, thereby likely reducing the overall emission of methane from tundra soils.

• Isolating a unique microbe from these iron-cycling communities, Rhodoferax, that is capable of both oxidizing and reducing iron. To date, all other iron cycling microbes belong to taxa that are capable of only oxidizing or reducing iron, but not doing both. We estimated that Rhodoferax is the most abundant microbe in the iron mats. Through sequencing its genome and studying its physiology using proteomic and transcriptomic approaches we have shown it possesses the biochemical capacity to carry out both oxidation and reduction.

In addition to these discoveries, we have taken advantage of an opportunity to collaborate with two artists, Kim and Philippe Villard, who have both resurrected and innovated a classic American woodblock art print, American Woodline Prints. Philippe traveled with the team to the Toolik Field Station where all this work was done and spent two weeks working with the scientists. The result is a series of unique art prints, the five senses and intuition, as well as the ‘Game of Iron’ an interactive card game based on both the science and artistic interpretation of the science team at work and capturing the greater meaning of the Arctic ecosystem. Works from this art will go on permanent display in a new Ocean Education and Innovation wing of Bigelow Laboratory that will be completed in early 2025.

Award Number 1754379

Previously we demonstrated that biological (primary) production in the Kuparuk River on the North Slope of Alaska (USA) is limited by exceedingly low concentrations of biologically useful phosphorus and that if we experimentally add phosphorus to streams, it profoundly alters the structure and function of these ecosystems. We assumed that the low concentration of phosphorus in these streams was caused by strong coupling of phosphorus production in tundra soils with high demand for phosphorus by tundra vegetation, so that little phosphorus was available to migrate to streams. However, it is not clear that tundra vegetation uses all the soil phosphorus available to it. We demonstrate that abundant concentrations of iron and aluminum create a substantial biogeochemical sink for phosphorus that sequesters P in forms that limit migration from the tundra to adjacent water bodies. We used two recently published pan-Arctic databases to infer that similar conditions may prevail in many other parts of the Arctic. We conclude that this biogeochemical control of phosphorus migration to headwater streams could be an important factor limiting primary production and therefore carbon processing in headwater streams in much of the Arctic, a finding that should be considered in regional and global models.

Background

The role of iron as a potential control on the mobility of phosphate (SRP) is well known in limnology, where the interaction between these two solutes in surficial sediments has been a subject of research on the vertical migration of phosphate from sediments to overlying water, for nearly 100 years.  However, until recently, there has been relatively little attention to how these same interactions might influence the lateral migration of phosphate from tundra to headwater streams and rivers in the Arctic.  This is important because we have previously established the low levels of phosphorus are likely to be the most important control (the limiting nutrient) on primary production in the Kuparuk River on the North Slope of Alaska. At the beginning of the Kuparuk River Long-Term experiment in the early 1980?s we hypothesized that as climate change warmed the Arctic region, thawing permafrost would release quantities of phosphorus that would exceed plant demand, and that the excess would migrate laterally to streams where it would significantly alter the food webs and trophic dynamics of Arctic stream ecosystems. Indeed, the Kuparuk River Long-Term phosphorus enrichment experiment was designed to study the effects of elevated phosphate levels in this river. Publications from this experiment have summarized results that show conclusively how an imposed release from phosphorus limitation significantly increases primary production and alters the community composition of primary producers and secondary consumers.  However, more recently we published data to show that while some nutrients (specifically nitrate and ammonium) have increased as the permafrost has thawed, phosphate has not and remains at near detection limits while total dissolved phosphorus concentrations have significantly declined. It has long been known that iron is abundant in tundra soils, constrained from migrating to deeper groundwater by the barrier imposed by permafrost. In this study, we showed that geochemical sequestration of phosphate by iron oxides supplements vegetation demand for this nutrient to effectively block lateral migration of phosphate to the Kuparuk River. While future thawing of permafrost will release more phosphate, it will also release more iron and aluminum, which will continue to interact with and sequester phosphate in this watershed. We then used a recent, public database of Arctic soil properties to show that these conditions may be widespread in the pan-Arctic region. This is a fundamentally different view of the likely impacts of permafrost thaw on Arctic streams and rivers and their role in nutrient and carbon transport and transformation. If control of phosphate migration to streams in rivers by geochemical sorption in the tundra is widespread in the Arctic, then it may affect approaches to research in Arctic stream ecology, estimates of riverine transport of solutes to the Arctic Ocean, and regional to global system modeling.

Key Points

1. Tundra soils in our study area have a high capacity to biogeochemically sequester and limit lateral migration of phosphorus.
2. This biogeochemical sequestration likely explains low phosphorus concentrations in adjacent streams, which limits stream primary production.
3. Using published data, we show that similar interactions may occur widely in the Arctic and may persist as permafrost continues to thaw.

Take home message: This project sheds light on an important interaction in the Arctic that has been overlooked and that could be important in projecting the effects of future climate warming on permafrost-dominated aquatic ecosystems.