192
Introduction
After publication of the original manuscript, the presented
method has been applied in various
15
N- and
13
C-labeling studies to
trace incorporation of
15
N and/or
13
C into bacterial and total microbial
biomass in different coastal sediments (Veuger et al. 2006, Veuger et
al. 2007, Veuger and Middelburg 2007). These applications and
analysis of the D-Ala content of some algal and cyanobacterial cul-
tures yielded valuable information regarding the interpretation of
15
N and
13
C incorporation into D-Ala and other hydrolysable amino
acids (HAAs), which is presented in this update.
Calculation of D/L-Ala ratio
In the original publication, the abundance of D-Ala was
expressed relative to that of L-Ala as D/L-Ala ratio (%) that
was calculated as D/L × 100. However, in most papers, the
abundance of D- versus L-AAs is presented as D/L (i.e., not %)
or as %D (D/(D + L) × 100) (e.g., McCarthy et al. 1998, Dittmar
et al. 2001, Amon et al. 2001, Kaiser and Benner 2005). To
prevent unnecessary confusion and for consistency, we now
also use D/L.
Hydrolysis-induced racemization
In the original publication, it was assumed that formation
of D-Ala from L-Ala by racemization during acid hydrolysis of
the samples was negligible compared to the amount of D-Ala
from bacteria. However, it is now clear that hydrolysis-
induced racemization yields substantial amounts of D-Ala and
hence should be corrected for. Recently, Kaiser and Benner
(2005) showed that liquid-phase hydrolysis of proteins and
algal biomass in 6 M HCl for 20 h at 110°C (same settings as
used in present method) yielded D/L-Ala ratios between 0.017
and 0.019. These values are very similar to those measured for
our axenic algal cultures (0.015–0.018, Table 4). Moreover, in
all
15
N- and
13
C-labeling experiments so far, excess
15
N and
13
C
D/L-Ala ratios were never <0.015, even for incubations of sur-
face sediment slurries in the light in which algal biomass was
an order of magnitude higher than bacterial biomass (Veuger
and Middelburg 2007). Altogether, these results indicate that
racemization during hydrolysis of microbial biomass (using
hydrolysis conditions as used in the present method) results in
D/L-Ala ratios of 0.015 to 0.02 (i.e., ~1.5% to 2% of L-Ala is con-
verted to D-Ala). Following Kaiser and Benner (2005), we used
these values to empirically correct our D-Ala data. Measured D-
Ala concentrations and excess label in D-Ala can be corrected
for hydrolysis-induced racemization as follows:
x bacterial D-Ala = [measured x D-Ala] – (0.017 × [measured x L-Ala])
where x is the concentration of excess
15
N or
13
C; 0.017 is used
as the average of the 0.015–0.02 range for hydrolysis-induced
racemization. When results are presented as D/L-Ala ratios
(concentrations of excess
15
N or
13
C), the most straightforward
way is to present measured (i.e., uncorrected) ratios and to
indicate the racemization background of 0.015–0.02 graphi-
cally (see Fig. 7).
Bacterial D/L-Ala ratios
In the original manuscript, we adopted the common assump-
tion that aquatic bacterial communities are dominated by Gram-
negative (G–) bacteria and hence that the D/L-Ala ratio of these
bacterial communities is similar to that for Gram negatives that
appear to have a relative uniform D/L-Ala ratio of ~0.05 (previ-
ously called 5%) (Table 2). However, some of the recent
15
N- and
13
C-labeling studies in sediments yielded excess
15
N and
13
C D/L-
Ala ratios up to ~0.1 (Veuger et al. 2006, Veuger et al. 2007,
Veuger and Middelburg 2007). These relatively high D/L-Ala
ratios appear to be due to substantial label incorporation by
Gram-positive (G+) bacteria and/or cyanobacteria, since these
are characterized by a thicker peptidoglycan layer (Madigan et al.
2000) and a corresponding higher D-Ala content and D/L-Ala
ratio. Although Gram negatives indeed appear to dominate bac-
terial communities in the water column, Gram positives have
been reported to contribute up to 30% of the total bacterial com-
munity in anaerobic subsurface sediment (Moriarty and Hayward
1982). This relatively high G+ abundance in deeper sediment is
consistent with increasing relative abundance of phospholipid-
derived fatty acids (PLFAs) characteristic for Gram positives with
Update of “Analysis of
15
N incorporation into D-alanine: A new
method for tracing nitrogen uptake by bacteria”
(Veuger et al. 2005, Limnol. Oceanogr. Methods 3:230-240)
Bart Veuger, Jack J. Middelburg, Henricus T. S. Boschker, and Marco Houtekamer
Centre for Estuarine and Marine Ecology, Netherlands Institute of Ecology (NIOO-KNAW), P.O. Box 140, 4400 AC Yerseke,
The Netherlands
Limnol. Oceanogr.: Methods 5, 2007, 192–194
© 2007, by the American Society of Limnology and Oceanography, Inc.
LIMNOLOGY
and
OCEANOGRAPHY: METHODS