Phosphorus, not nitrogen, limits plants and microbial primary producers following glacial retreat.

Current models of ecosystem development hold that low nitrogen availability limits the earliest stages of primary succession, but these models were developed from studies conducted in areas with temperate or wet climates. Global warming is now causing rapid glacial retreat even in inland areas with cold, dry climates, areas where ecological succession has not been adequately studied. We combine field and microcosm studies of both plant and microbial primary producers and show that phosphorus, not nitrogen, is the nutrient most limiting to the earliest stages of primary succession along glacial chronosequences in the Central Andes and central Alaska. We also show that phosphorus addition greatly accelerates the rate of succession for plants and for microbial phototrophs, even at the most extreme deglaciating site at over 5000 meters above sea level in the Andes of arid southern Peru. These results challenge the idea that nitrogen availability and a severe climate limit the rate of plant and microbial succession in cold-arid regions and will inform conservation efforts to mitigate the effects of global change on these fragile and threatened ecosystems.

Nutrient limitation of soil microbial activity during the earliest stages of ecosystem development.

A dominant paradigm in ecology is that plants are limited by nitrogen (N) during primary succession. Whether generalizable patterns of nutrient limitation are also applicable to metabolically and phylogenetically diverse soil microbial communities, however, is not well understood. We investigated if measures of N and phosphorus (P) pools inform our understanding of the nutrient(s) most limiting to soil microbial community activities during primary succession. We evaluated soil biogeochemical properties and microbial processes using two complementary methodological approaches-a nutrient addition microcosm experiment and extracellular enzyme assays-to assess microbial nutrient limitation across three actively retreating glacial chronosequences. Microbial respiratory responses in the microcosm experiment provided evidence for N, P and N/P co-limitation at Easton Glacier, Washington, USA, Puca Glacier, Peru, and Mendenhall Glacier, Alaska, USA, respectively, and patterns of nutrient limitation generally reflected site-level differences in soil nutrient availability. The activities of three key extracellular enzymes known to vary with soil N and P availability developed in broadly similar ways among sites, increasing with succession and consistently correlating with changes in soil total N pools. Together, our findings demonstrate that during the earliest stages of soil development, microbial nutrient limitation and activity generally reflect soil nutrient supply, a result that is broadly consistent with biogeochemical theory.

Nutrient addition dramatically accelerates microbial community succession.

The ecological mechanisms driving community succession are widely debated, particularly for microorganisms. While successional soil microbial communities are known to undergo predictable changes in structure concomitant with shifts in a variety of edaphic properties, the causal mechanisms underlying these patterns are poorly understood. Thus, to specifically isolate how nutrients--important drivers of plant succession--affect soil microbial succession, we established a full factorial nitrogen (N) and phosphorus (P) fertilization plot experiment in recently deglaciated (∼3 years since exposure), unvegetated soils of the Puca Glacier forefield in Southeastern Peru. We evaluated soil properties and examined bacterial community composition in plots before and one year after fertilization. Fertilized soils were then compared to samples from three reference successional transects representing advancing stages of soil development ranging from 5 years to 85 years since exposure. We found that a single application of +NP fertilizer caused the soil bacterial community structure of the three-year old soils to most resemble the 85-year old soils after one year. Despite differences in a variety of soil edaphic properties between fertilizer plots and late successional soils, bacterial community composition of +NP plots converged with late successional communities. Thus, our work suggests a mechanism for microbial succession whereby changes in resource availability drive shifts in community composition, supporting a role for nutrient colimitation in primary succession. These results suggest that nutrients alone, independent of other edaphic factors that change with succession, act as an important control over soil microbial community development, greatly accelerating the rate of succession.

Fumarole-supported islands of biodiversity within a hyperarid, high-elevation landscape on Socompa Volcano, Puna de Atacama, Andes.

Fumarolic activity supports the growth of mat-like photoautotrophic communities near the summit (at 6,051 m) of Socompa Volcano in the arid core of the Andes mountains. These communities are isolated within a barren, high-elevation landscape where sparse vascular plants extend to only 4,600 m. Here, we combine biogeochemical and molecular-phylogenetic approaches to characterize the bacterial and eucaryotic assemblages associated with fumarolic and nonfumarolic grounds on Socompa. Small-subunit rRNA genes were PCR amplified, cloned, and sequenced from two fumarolic soil samples and two reference soil samples, including the volcanic debris that covers most of the mountain. The nonfumarolic, dry, volcanic soil was similar in nutrient status to the most extreme Antarctic Dry Valley or Atacama Desert soils, hosted relatively limited microbial communities dominated by Actinobacteria and Fungi, and contained no photoautotrophs. In contrast, modest fumarolic inputs were associated with elevated soil moisture and nutrient levels, the presence of chlorophyll a, and (13)C-rich soil organic carbon. Moreover, this soil hosted diverse photoautotroph-dominated assemblages that contained novel lineages and exhibited structure and composition comparable to those of a wetland near the base of Socompa (3,661-m elevation). Fumarole-associated eucaryotes were particularly diverse, with an abundance of green algal lineages and a novel clade of microarthropods. Our data suggest that volcanic degassing of water and (13)C-rich CO(2) sustains fumarole-associated primary producers, leading to a complex microbial ecosystem within this otherwise barren landscape. Finally, we found that human activities have likely impacted the fumarolic soils and that fumarole-supported photoautotrophic communities may be exceptionally sensitive to anthropogenic disturbance.

Microbial community succession in an unvegetated, recently deglaciated soil.

Primary succession is a fundamental process in macroecosystems; however, if and how soil development influences microbial community structure is poorly understood. Thus, we investigated changes in the bacterial community along a chronosequence of three unvegetated, early successional soils ( approximately 20-year age gradient) from a receding glacier in southeastern Peru using molecular phylogenetic techniques. We found that evenness, phylogenetic diversity, and the number of phylotypes were lowest in the youngest soils, increased in the intermediate aged soils, and plateaued in the oldest soils. This increase in diversity was commensurate with an increase in the number of sequences related to common soil bacteria in the older soils, including members of the divisions Acidobacteria, Bacteroidetes, and Verrucomicrobia. Sequences related to the Comamonadaceae clade of the Betaproteobacteria were dominant in the youngest soil, decreased in abundance in the intermediate age soil, and were not detected in the oldest soil. These sequences are closely related to culturable heterotrophs from rock and ice environments, suggesting that they originated from organisms living within or below the glacier. Sequences related to a variety of nitrogen (N)-fixing clades within the Cyanobacteria were abundant along the chronosequence, comprising 6-40% of phylotypes along the age gradient. Although there was no obvious change in the overall abundance of cyanobacterial sequences along the chronosequence, there was a dramatic shift in the abundance of specific cyanobacterial phylotypes, with the intermediate aged soils containing the greatest diversity of these sequences. Most soil biogeochemical characteristics showed little change along this approximately 20-year soil age gradient; however, soil N pools significantly increased with soil age, perhaps as a result of the activity of the N-fixing Cyanobacteria. Our results suggest that, like macrobial communities, soil microbial communities are structured by substrate age, and that they, too, undergo predictable changes through time.