Extracellular enzymes produced by het- erotrophic microbial communities are major drivers of carbon and nutrient cycling in terrestrial, freshwater, and marine environments. Although carbon and nutrient cycles are coupled on global scales, studies of extracellular enzymes associated with terrestrial, freshwater, and marine microbial communities are not often compared across ecosystems. In part, this disconnect arises because the environmental parame- ters that control enzyme activities in terrestrial and freshwater systems, such as temperature, pH, and moisture content, have little explanatory power for patterns of enzyme activities in marine systems. Instead, factors such as the functional diversity of microbial communities may explain varying patterns of enzyme activities observed in the ocean to date. In any case, many studies across systems focus on similar issues that highlight the commonalities of microbial community organization. Examples include the effec- tive lifetime of enzymes released into the environ- ment; the extent to which microbial communities coordinate enzyme expression to decompose complex organic substrates; and the influence of microbial community composition on enzyme activities and kinetics. Here we review the often-disparate research foci in terrestrial, freshwater, and marine environ- ments. We consider the extent to which environmental factors may regulate extracellular enzyme activities within each ecosystem, and highlight commonalities and current methodological challenges to identify

Extracellular enzymes in terrestrial, freshwater, and marine environments: perspectives on system variability and common research needs

Focusing on Sumatra, a hotspot of tropical lowland rainforest transformation, we investigated effects of the con- version of rainforests into rubber agroforests (Bjungle rubber^), intensive rubber, and oil palm plantations on the communities of litter and soil microorganisms and identified factors responsible for these changes. Litter basal respiration, microbial biomass, total bacterial phospholipid fatty acids (PLFAs), and fungal PLFAs did not vary significantly with rainforest conversion. In litter of converted ecosystems, the concentration of certain PLFAs including the Gram-negative bacteria marker PLFA cy17:0 and the Gram-positive bacteria marker PLFA i17:0 was reduced as compared to rainforest, whereas the concentration of the arbuscular mycorrhizal fungi (AMF) marker neutral lipid fatty acid (NLFA) 16:1ω5c in- creased. As indicated by redundancy analysis, litter pH and carbon concentration explained most of the variation in litter microbial community composition. In soil, microbial biomass did not vary significantly with rainforest conversion, whereas basal respiration declined. Total PLFAs and especially that of Gram-negative bacteria decreased, whereas PLFA i17:0 in- creased with rainforest conversion. The concentration of fun- gal PLFAs increased with rainforest conversion, whereas NLFA 16:1ω5c did not change significantly. Redundancy analysis indicated that soil pH explained most of the variation in soil microbial community composition. Overall, the data suggest that conversion of rainforests into production systems results in more pronounced changes in microbial community composition in soil as compared to litter. In particular, the response of fungi and bacteria was more pronounced in soil, while the response of AMF was more pronounced in litter. Notably, only certain bacterial markers but not those of saprotrophic fungi and AMF were detrimentally affected by rainforest conversion.

Impact of tropical lowland rainforest conversion into rubber and oil palm plantations on soil microbial communities

Terrestrial ecosystems have experienced rising nitrogen (N) inputs during the last decades with consequences for belowground carbon (C) and N dynamics. This study investigates how long-term N and phosphorus (P) additions affect microbial community composition, and to what extent microbial homeostasis explains changes in different processes involved in soil C and N cycling in response to nutrient addition. We studied a 66-year-old nutrient addition experiment in a mesic grassland in South Africa, consisting of four different levels of N addition (0, 7, 14, and 21 g N m−2 yr−1) with and without P addition (0, and 9 g P m−2 yr−1). Despite strong changes in the microbial community (observed through 16S rRNA gene and ITS amplicon sequencing), the microbial biomass C:N ratio did not change. N addition decreased microbial N acquisition as indicated by reduced leucine-aminopeptidase activity, and increased microbial net N mineralization. In contrast, predicted relative abundances of functional genes involved in degradation of labile C compounds (e.g. cellulose, hemicellulose, and chitin) as well as β-glucosidase and N-acetylglucosaminidase activities increased with elevated N availability. In combination, this pointed to a more intensive investment of microorganisms into C acquisition upon N addition. In contrast, N addition and associated soil acidification decreased microbial biomass and respiration and altered the community composition with prokaryotes being more affected than fungi. Nitrogen addition increased the relative abundance of gram-positive over gram-negative bacteria and favored taxa with low genome-size. Taken together, our findings support the concept that C and N cycling processes can be explained by the property of the soil microbial community to keep the element ratio of its biomass constant and by its reaction to soil acidification. Our findings suggest that predicted elevated N inputs might largely shape soil C and N cycling because the soil microbial community adjusts metabolic processes, which allows it to maintain its biomass stoichiometry constant.

Stoichiometric controls of soil carbon and nitrogen cycling after long-term nitrogen and phosphorus addition in a mesic grassland in South Africa

Half a century ago in an Amazonian rainforest, Went and Stark [1, 2] observed ‘endotrophic mycorrhizal’ hyphae proliferating in leaf litter adjacent to mycorrhizal roots. They inferred the fungi were accessing, and subsequently transferring, litter-bound mineral nutrients to host plants in a phenomenon they called ‘direct mineral cycling.’ This hypothesis was consistent with acceptance of fungi as primary decomposers in forest ecosystems and mycorrhizal fungi as symbionts that transfer mineral nutrients (hereafter, ‘nutrients’) to host plants. ‘Endotrophic mycorrhizas,’ as used by those authors, were later termed ‘arbuscular mycorrhizas’ and involve a phylogenetically distinct group of fungi from the phylum Glomeromycota [3]. Early observations of arbuscular mycorrhizal (AM) fungi proliferating in organic matter led researchers to surmise saprotrophic capabilities [4–6]. However, attempts to culture AM fungi independent of host plants were unsuccessful, and researchers now understand AM fungi as obligate symbionts entirely dependent on host plant roots for carbon [7, 8]. In fact, AM fungi appear incapable of producing the lytic enzymes necessary to cleave organic molecules [9, 10] and evidence still largely, but not universally, suggests these fungi are limited to assimilating inorganic forms of nutrients (nitrogen reviewed by Hodge and Storer [11]; phosphorus by Smith et al. [12]). Thus, AM fungi alone are unlikely to access litter-bound nutrients as Went and Stark [1, 2] originally envisioned, and ‘direct mineral cycling’ has languished in the bin of unsupported hypotheses. Yet AM fungi colonize litter in a variety of habitats (Table 1), and AM host plants are often successful in organic soils despite predictions that these plants are largely restricted to mineral soils where inorganic nutrients predominate [13, 14]. In this Perspective, we argue for a reconsideration of the ‘direct mineral cycling’ hypothesis; not because we believe that these fungi can directly mobilize organically bound nutrients, but because of ample evidence that AM fungi can influence degradation of organic matter and subsequently acquire and transfer a portion of released nutrients to their associated host plants [15, 16]. Therefore, the functional consequences of AM fungi growing into leaf litter may match those of ‘direct mineral cycling.’ We review the literature and present new data that unequivocally show rapid colonization by AM fungi inside dead leaves in coniferous-dominated forests in the Pacific Northwest. Thus, we argue that AM fungal colonization of litter and not-yet-decomposed plant matter may be a global phenomenon that could have far-reaching implications for plant–plant interactions and nutrient cycling in both natural and managed ecosystems. Finally, we outline a set of questions that we hope will spur crossdisciplinary research into what we believe is an often overlooked and under-researched topic.

/pdf/revisiting-the-direct-mineral-cycling-hypothesis-arbuscular-1ph63rk4hh.pdf

Revisiting the 'direct mineral cycling' hypothesis: arbuscular mycorrhizal fungi colonize leaf litter, but why?

In the tropical rainforest of Amazonia, phosphorus (P) is one of the main nutrients controlling forest dynamics, but its effects on the future of the forest biomass carbon (C) storage under elevated atmospheric CO2 concentrations remain uncertain. Soils in vast areas of Amazonia are P impoverished, and little is known about the variation or plasticity in plant P-use and -acquisition strategies across space and time, hampering the accuracy of projections in vegetation models. Here, we synthesize the current knowledge of leaf P resorption, fine-root P foraging, arbuscular mycorrhizal symbioses, and root acid phosphatase and organic acid exudation and discuss how these strategies vary with soil P concentrations and in response to elevated atmospheric CO2 . We identify knowledge gaps and suggest ways forward to fill those gaps. Additionally, we propose a conceptual framework for the variations in plant P-use and -acquisition strategies along soil P gradients of Amazonia. We suggest that in soils with intermediate to high P concentrations, at the plant community level, investments are primarily directed to P foraging strategies via roots and arbuscular mycorrhizas, whereas, in soils with intermediate to low P concentrations, investments shift to prioritize leaf P resorption and mining strategies via phosphatases and organic acids.

Plant phosphorus-use and -acquisition strategies in Amazonia.

Relationships between the litter colonization by saprotrophic and arbuscular mycorrhizal fungi with depth in a tropical forest.

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Relationships between the litter colonization by saprotrophic and arbuscular mycorrhizal fungi with depth in a tropical forest.