Abstract. Oceanic bacterial communities process a major fraction of marine organiccarbon. A substantial portion of this carbon transformation occurs in themesopelagic zone, and a further fraction fuels bacteria in the bathypelagiczone. However, the capabilities and limitations of the diverse microbialcommunities at these depths to degrade high-molecular-weight (HMW) organicmatter are not well constrained. Here, we compared the responses of distinctmicrobial communities from North Atlantic epipelagic (0–200 m), mesopelagic(200–1000 m), and bathypelagic (1000–4000 m) waters at two open-oceanstations to the same input of diatom-derived HMW particulate and dissolvedorganic matter. Microbial community composition and functional responses tothe input of HMW organic matter – as measured by polysaccharide hydrolase,glucosidase, and peptidase activities – were very similar between thestations, which were separated by 1370 km but showed distinct patterns withdepth. Changes in microbial community composition coincided with changes inenzymatic activities: as bacterial community composition changed in responseto the addition of HMW organic matter, the rate and spectrum of enzymaticactivities increased. In epipelagic mesocosms, the spectrum of peptidaseactivities became especially broad and glucosidase activities were veryhigh, a pattern not seen at other depths, which, in contrast, were dominatedby leucine aminopeptidase and had much lower peptidase and glucosidase ratesin general. The spectrum of polysaccharide hydrolase activities was enhancedparticularly in epipelagic and mesopelagic mesocosms, with fewerenhancements in rates or spectrum in bathypelagic waters. The timing andmagnitude of these distinct functional responses to the same HMW organicmatter varied with depth. Our results highlight the importance of residencetimes at specific depths in determining the nature and quantity of organicmatter reaching the deep sea.
more »
« less
Community structural differences shape microbial responses to high molecular weight organic matter
The extent to which differences in microbial community structure result in variations in organic matter (OM) degradation is not well understood. Here, we tested the hypothesis that distinct marine microbial communities from North Atlantic surface and bottom waters would exhibit varying compositional succession and functional shifts in response to the same pool of complex high molecular weight (HMW‐OM). We also hypothesized that microbial communities would produce a broader spectrum of enzymes upon exposure to HMW‐OM, indicating a greater potential to degrade these compounds than reflected by initial enzymatic activities. Our results show that community succession in amended mesocosms was congruent with cell growth, increased bacterial production and most notably, with substantial shifts in enzymatic activities. In all amended mesocosms, closely related taxa that were initially rare became dominant at time frames during which a broader spectrum of active enzymes were detected compared to initial timepoints, indicating a similar response among different communities. However, succession on the whole‐community level, and the rates, spectra and progression of enzymatic activities, reveal robust differences among distinct communities from discrete water masses. These results underscore the crucial role of rare bacterial taxa in ocean carbon cycling and the importance of bacterial community structure for HMW‐OM degradation.
more » « less- Award ID(s):
- 1736772
- PAR ID:
- 10462669
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Environmental Microbiology
- Volume:
- 21
- Issue:
- 2
- ISSN:
- 1462-2912
- Page Range / eLocation ID:
- p. 557-571
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Heterotrophic bacteria initiate the degradation of high molecular weight organic matter by producing an array of extracellular enzymes to hydrolyze complex organic matter into sizes that can be taken up into the cell. These bacterial communities differ spatially and temporally in composition, and potentially also in their enzymatic complements. Previous research has shown that particle-associated bacteria can be considerably more active than bacteria in the surrounding bulk water, but most prior studies of particle-associated bacteria have been focused on the upper ocean - there are few measurements of enzymatic activities of particle-associated bacteria in the mesopelagic and bathypelagic ocean, although the bacterial communities in the deep are dependent upon degradation of particulate organic matter to fuel their metabolism. We used a broad suite of substrates to compare the glucosidase, peptidase, and polysaccharide hydrolase activities of particle-associated and unfiltered seawater microbial communities in epipelagic, mesopelagic, and bathypelagic waters across 11 stations in the western North Atlantic. We concurrently determined bacterial community composition of unfiltered seawater and of samples collected via gravity filtration (>3 μm). Overall, particle-associated bacterial communities showed a broader spectrum of enzyme activities compared with unfiltered seawater communities. These differences in enzymatic activities were greater at offshore than at coastal locations, and increased with increasing depth in the ocean. The greater differences in enzymatic function measured on particles with depth coincided with increasing differences in particle-associated community composition, suggesting that particles act as ‘specialty centers’ that are essential for degradation of organic matter even at bathypelagic depths.more » « less
-
more » « less
Abstract Increasing glacial discharge can lower salinity and alter organic matter (OM) supply in fjords, but assessing the biogeochemical effects of enhanced freshwater fluxes requires understanding of microbial interactions with OM across salinity gradients. Here, we examined microbial enzymatic capabilities—in bulk waters (nonsize‐fractionated) and on particles (≥ 1.6
μ m)—to hydrolyze common OM constituents (peptides, glucose, polysaccharides) along a freshwater–marine continuum within Tyrolerfjord‐Young Sound. Bulk peptidase activities were up to 15‐fold higher in the fjord than in glacial rivers, whereas bulk glucosidase activities in rivers were twofold greater, despite fourfold lower cell counts. Particle‐associated glucosidase activities showed similar trends by salinity, but particle‐associated peptidase activities were up to fivefold higher—or, for several peptidases, only detectable—in the fjord. Bulk polysaccharide hydrolase activities also exhibited freshwater–marine contrasts: xylan hydrolysis rates were fivefold higher in rivers, while chondroitin hydrolysis rates were 30‐fold greater in the fjord. Contrasting enzymatic patterns paralleled variations in bacterial community structure, with most robust compositional shifts in river‐to‐fjord transitions, signifying a taxonomic and genetic basis for functional differences in freshwater and marine waters. However, distinct dissolved organic matter (DOM) pools across the salinity gradient, as well as a positive relationship between several enzymatic activities and DOM compounds, indicate that DOM supply exerts a more proximate control on microbial activities. Thus, differing microbial enzymatic capabilities, community structure, and DOM composition—interwoven with salinity and water mass origins—suggest that increased meltwater may alter OM retention and processing in fjords, changing the pool of OM supplied to coastal Arctic microbial communities. -
more » « less
Abstract Heterotrophic microbes initiate the degradation of high molecular weight organic matter using extracellular enzymes. Our understanding of differences in microbial enzymatic capabilities, especially among particle‐associated taxa and in the deep ocean, is limited by a paucity of hydrolytic enzyme activity measurements. Here, we measured the activities of a broad range of hydrolytic enzymes (glucosidases, peptidases, polysaccharide hydrolases) in epipelagic to bathypelagic bulk water (nonsize‐fractionated), and on particles (≥ 3
μ m) along a 9800 km latitudinal transect from 30°S in the South Pacific to 59°N in the Bering Sea. Individual enzyme activities showed heterogeneous latitudinal and depth‐related patterns, with varying biotic and abiotic correlates. With increasing latitude and decreasing temperature, lower laminarinase activities sharply contrasted with higher leucine aminopeptidase (leu‐AMP) and chondroitin sulfate hydrolase activities in bulk water. Endopeptidases (chymotrypsins, trypsins) exhibited patchy spatial patterns, and their activities can exceed rates of the widely measured exopeptidase, leu‐AMP. Compared to bulk water, particle‐associated enzymatic profiles featured a greater relative importance of endopeptidases, as well as a broader spectrum of polysaccharide hydrolases in some locations, and latitudinal and depth‐related trends that are likely consequences of varying particle fluxes. As water depth increased, enzymatic spectra on particles and in bulk water became narrower, and diverged more from one another. These distinct latitudinal and depth‐related gradients of enzymatic activities underscore the biogeochemical consequences of emerging global patterns of microbial community structure and function, from surface to deep waters, and among particle‐associated taxa. -
more » « less
Abstract Many soils are deep, yet soil below 20 cm remains largely unexplored. Exotic plants can have shallower roots than native species, so their impact on microorganisms is anticipated to change with depth. Using environmental
DNA and extracellular enzymatic activities, we studied fungal and bacterial community composition, diversity, function, and co‐occurrence networks between native and exotic grasslands at soil depths up to 1 m. We hypothesized (1) the composition and network structure of both fungal and bacterial communities will change with increasing depth, and diversity and enzymatic function will decrease; (2) microbial enzymatic function and network connectedness will be lower in exotic grasslands; and (3) irrigation will alter microbial networks, increasing the overall connectedness. Microbial diversity decreased with depth, and community composition wasdistinctly different between shallow and deeper soil depths with higher numbers of unknown taxa in lower soil depths. Fungal communities differed between native and exotic plant communities. Microbial community networks were strongly shaped by biotic and abiotic factors concurrently and were the only microbial measurement affected by irrigation. In general, fungal communities were more connected in native plant communities than exotic, especially below 10 cm. Fungal networks were also more connected at lower soil depths albeit with fewer nodes. Bacterial communities demonstrated higher complexity, and greater connectedness and nodes, at lower soil depths for native plant communities. Exotic plant communities’ bacterial network connectedness altered at lower soil depths dependent on irrigation treatments. Microbial extracellular enzyme activity for carbon cycling enzymes significantly declined with soil depth, but enzymes associated with nitrogen and phosphorus cycling continued to have similar activities up to 1 m deep. Our results indicate that native and exotic grasslands have significantly different fungal communities in depths up to 1 m and that both fungal and bacterial networks are strongly shaped jointly by plant communities and abiotic factors. Soil depth is independently a major determinant of both fungal and bacterial community structures, functions, and co‐occurrence networks and demonstrates further the importance of including soil itself when investigating plant–microbe interactions.
