Organic substrate quality as the link between bacterioplankton carbon demand and growth efficiency in a temperate salt-marsh estuary

Abstract

Bacterioplankton communities play a key role in aquatic carbon cycling, specifically with respect to the magnitude of organic carbon processed and partitioning of this carbon into biomass and respiratory losses. Studies of bacterioplankton carbon demand (BCD) and growth efficiency (BGE) frequently report higher values in more productive systems, suggesting these aspects of carbon metabolism may be positively coupled. However, the existence of such a relationship in natural aquatic systems has yet to be identified. Using a comprehensive 2-year study of bacterioplankton carbon metabolism in a temperate estuary, we investigated BCD and BGE and explored factors that may modulate their magnitude and coherence, including nutrient concentrations, dissolved nutrient uptake and source and quality of dissolved organic carbon (DOC). During the course of our study, BCD ranged from 0.4 to 15.9 lg l À1 h -1, with an overall mean of 3.8 lg l À1 h -1. Mean BGE was similar to that reported for other estuarine systems (0.32) and of comparable range (that is, 0.06-0.68). Initial analyses identified a negative correlation between BCD and BGE, yet removal of the effect of temperature revealed an underlying positive coupling that was also correlated with long-term DOC lability. Whereas BCD was weakly related to ambient DOC concentrations, neither BCD nor BGE showed any relationship with ambient nutrient concentrations or nutrient uptake stoichiometries. We conclude that in this carbon-rich estuary, organic matter source and quality play an important role in regulating the magnitude of carbon metabolism and may be more important than nutrient availability alone in the regulation of BGE.

Bacterial carbon demand and growth efficiency in a coastal upwelling system

“…Previous studies have indicated that BGE varies greatly depending on environmental factors such as nutrient availability (Rivkin & Anderson 1997), DOM quality (Goldman et al 1987, Lemée et al 2002, Reinthaler & Herndl 2005, Apple & del Giorgio 2007 and temperature (Rivkin & Legendre, 2001). Our data suggest that the BGE in the Ría de Vigo is partly controlled by inorganic nutrient availability and by the quality of the BDOM substrate (Fig.…”

High bacterial carbon demand and low growth efficiency at a tropical hypereutrophic estuary: importance of dissolved organic matter remineralization

“…The high variability in BP, BR, BCD and BGE, also observed in other tropical estuaries (GUENTHER et al, 2008;RAM et al, 2007), was already expected due to the high hydrodynamic complexity of this system (GUENTHER et al, 2015). Although the BP rates measured in Recife harbor were similar, on average, to other tropical and temperate estuaries (APPLE; DEL GIORGIO, 2007;NEWELL, 2012;GUENTHER et al, 2008;RAM et al, 2003), the BR rates were higher, leading to lower BGE (see Table 3). Bacterial respiration rates were more variable than BP rates and inversely correlated to BGE (see Table 2) which suggest that BGE variations are better explained by BR.…”

“…The direct correlation between BP and N-NH 4 (r=0.53; p=0.01) and the absence of correlation between BP and the N-oxidized forms (r=0.25; p=0.23) suggests a higher reliability of bacterioplankton on ammonium contents in this system. The higher BGE observed in the more productive estuarine systems is usually correlated to the nutrient availability and/or DOM quality (APPLE; DEL GIORGIO, 2007;ASMALA et al, 2014;NEWELL, 2012;GUENTHER et al, 2008) which support bacterial growth (BP) with less maintenance energy costs (BR). The DOM quality (or lability) is defined by its nutritional value (stoichiometric balanced C:N:P ratio), diagenetic state (freshly leached vs. microbial processed), as well as molecular size (low vs. high molecular weight) and shape (degree of aromaticity), irrespective of its allochthonous or autochthonous origin (AMON; BENNER, 1996;ATTERMEYER et al, 2014;GOLDMAN et al, 1987).…”

“…Nevertheless, several studies showed a great spatial and temporal variability in BGE within and among systems, due to several abiotic and biotic factors like temperature, inorganic nutrients availability, dissolved organic matter (DOM) quality, light incidence and grazing pressure (APPLE; DEL GIORGIO, 2007;APPLE et al, 2006;ASMALA et al, 2014;BERGGREN et al, 2010;CORY et al, 2010;RAM et al, 2003). The need for simultaneous in situ estimates of bacterial production and respiration rates became thus imperative to accurately evaluate the bacterial carbon metabolism in the aquatic systems and understand its regulation.…”

Changing Bacterial Growth Efficiencies across a Natural Nutrient Gradient in an Oligotrophic Estuary

“…Eiler et al (2003) found that DOC concentration correlates with BGE in an asymptotic pattern, suggesting that DOC concentration affects BGE only in the most oligotrophic conditions. A study by Apple and del Giorgio (2007) showed that BGE positively correlated with long-term DOC lability in a temperate estuary, indicating that dissolved organic matter (DOM) source (quality) may impact BGE. A study conducted by Lennon and Pfaff (2005) showed that DOM with low C:P ratios (less than 160:1 by mol) from different sources was associated with high bacterial productivity, indicating that P availability can affect BGE values.…”