Relationship of bacterial growth efficiency to spatial variation in bacterial activity in the Hudson River

Abstract

Variation in bacterial production (BP) is used as an indicator of bacterial metabolism and carbon processing in the analysis of aquatic ecosystems. The allocation of carbon by bacteria to either BP or respiration (BR), however, is variable and may potentially influence the assessment of carbon cycling by bacteria in ecosystems. We studied 10 transects in the Hudson River estuary where there is a gradient in BP and BR along the flow path of the estuary. We measured BP and BR in filtered samples to derive an estimate of bacterial growth efficiency (BGE) that we could compare with independent measurements of total BP (BP T ) from unfiltered samples to evaluate the relationship of BGE to BP. We further tested the assumption that BGE derived from filtered samples is a good estimator of the ambient BGE on a subset of transects in the upriver section where bacteria dominate respiration. There was good agreement (near 1:1) between respiration measured in unfiltered samples and total BR estimated from BP T and BGE in the filtered fraction (total BR = [BP T /BGE] -BP T ). BGE averaged 0.29 but varied from 0.07 to 0.61, and did not explain the general decline in BP T along the river. Rather, BGE was strongly correlated to the residuals of the BP T and specific BP T (i.e. growth) vs. flow path (= river kilometer) relationship, indicating that shifts in bacterial carbon allocation explained local variations in bacterial metabolic activity, and these shifts were superimposed on the larger scale decline in carbon consumption and BP. The pattern in BP along the Hudson River is clearly a combination of changes in consumption as well as in BGE, to the point that the pattern in BP T or growth would be impossible to recreate from any one of these 2 components. We conclude that BGE indicates changes in carbon allocation of bacteria that reflect shifts in relative BR and BP at shorter time and space scales that are distinct from larger overall patterns in consumption and BP.

Coherent patterns in bacterial growth, growth efficiency, and leucine metabolism along a northeastern Pacific inshore‐offshore transect

“…In this regard, it has been postulated that growth efficiency and growth rate should be coupled (Vallino et al 1996;del Giorgio and Cole 2000) such that high growth rates should generally coincide with higher growth efficiencies. On the other hand, it has generally been assumed that substrate consumption and growth should be coupled (Church 2008).…”

“…Exceptions to this may occur, for example, when consumption of C may be transiently impeded by nutrient limitation or even grazing (Thingstad et al 1997;Obernosterer et al 2003;Gasol et al 2009). But because the chemical nature of the available C varies spatially and temporally in marine systems, a given rate of bulk C consumption may result in very different energy yields, nutrients, and C precursors for biosynthesis (Linton and Stephenson 1978;del Giorgio and Cole 2000). In addition, the energetic demands of bacterial cells themselves are not constant such that for any given rate of C consumption, bacteria may experience different degrees of energy limitation (del Giorgio and Gasol 2008).…”

“…The notion of a single regulating factor of marine bacterioplankton growth is clearly an oversimplification (Saito et al 2008) that does not capture the complexity of the regulation of bacterial activity in the ocean. For example, various types of nutrient limitation have been shown to influence BGE (Tortell et al 1996;del Giorgio and Cole 2000). However, nutrients may profoundly influence bacterial growth even if they are not limiting from a stoichiometric point of view.…”

“…Marine bacteria collectively maximize their survival and growth not by adjusting any single aspect of C metabolism but most likely by simultaneously modulating different aspects of their overall metabolism (Carlson et al 2007;del Giorgio and Gasol 2008). For example, bioenergetic considerations would suggest that growth rate and bacterial growth efficiency (BGE) should be related to each other (del Giorgio and Cole 2000) and that both should in turn be related to the ratio of leucine to thymidine incorporation (Leu : TdR ratio), which provides an index of the relative importance of protein vs. nucleic acid synthesis and thus of the degree to which growth is balanced or unbalanced (Chin-Leo and Kirchman 1990;Gasol et al 1998). In turn, C processing and the subsequent growth should be linked to the underlying C availability and consumption (Church 2008).…”

“…These components of metabolism have been generally measured individually but have then often been used to infer other aspects of bacterial C metabolism and overall performance within the system, yet these extrapolations are problematic. For example, estimates of bacterial production (BP) have been extensively used to infer total bacterial C consumption in the oceans (Carlson and Ducklow 1996;Ducklow 2000;Gasol et al 2008), but this link is mediated by BGE, which is now recognized as being much more variable and less predictable than was originally assumed (Jahnke and Craven 1995;del Giorgio and Cole 2000). Studies that have attempted to measure BGE directly in ocean samples have reported low BGE values, usually in the range of 1% to 20% (Biddanda et al 1994;Sherry et al 2002;Alonso-Sá ez et al 2007).…”