At a time when metagenomic studies are
capturing the limelight, why is culturing
important? In short, cultures are important
because they provide complete genomes and
the means to test the hypotheses that emerge
from genomic data. Cultured bacterial and
archaeal isolates that have yielded complete
genome sequences have also proved to be
important for evaluating metagenomic data
— a recent paper that presented environ-
mental whole-genome shotgun-sequencing
data from Craig Venter’s Global Ocean
Survey relied heavily on complete genome
sequences from bacterial plankton to evaluate
metagenomic data, because procedures for
reconstructing genomes from whole-genome
shotgun sequences are not yet reliable
1,2
.
Cultures, supported by predictions from
genomes, together with the information
about natural variation that is provided by
metagenomics are a powerful combination.
On the one hand, live cells allow the study
of the whole organism, rather than trying to
infer physiological properties from an incom-
plete list of parts. On the other hand, genomic
and metagenomic data can reveal hidden
metabolic potential, metabolic pathways,
regulatory circuits and conservation among
cultured and uncultured bacteria (FIG. 1).
The TIMELINE lists selected important
events in marine microbial cultivation.
Historically, there has been debate about
whether heterotrophic microbial cells can
grow at the extremely low nutrient concentra-
tions that are found in natural ecosystems
3
.
However, now there are many strains that
have been cultured which replicate well in
sterilized seawater, but do not grow in media
that contain concentrated organic nutrients
(BOX 1). The main challenge of designing
artificial media to mimic natural seawater is
the accurate reconstruction of the complex
composition of dissolved organic carbon
(DOC) and trace elements (TABLE 1). To easily
obtain dense, turbid bacterial or archaeal cul-
tures, most researchers have relied on media
that contain high concentrations of organic
carbon. ZoBell’s Marine Medium
4
, which is
still widely used for culturing heterotrophic
bacteria, has 170-fold more DOC than natu-
ral seawater. To make matters worse, most of
the DOC in seawater is derived from recalci-
trant matter, so that the difference in useable
organic carbon probably exceeds three orders
of magnitude (TABLE 1).
The first culture of an obligate oligotroph
was obtained from a freshwater sample in
1981 (REF. 5). In the same year, an influential
review of oligotrophy was published
6
.
Subsequently, several research groups, most
notably that of Don Button, developed
methods for the successful cultivation of
oligotrophs and began working with cultures
of marine bacteria that could be grown in
autoclaved seawater
7–9
. The laboratory of
S.G. modified Button’s methods by redu-
cing the size of cultures to microtitre dish
volumes, implementing screening methods
and adopting clean procedures that had
been developed by oceanographers for han-
dling seawater
10
. Additional modifications
included segregating containers that were
used for culturing cells, avoiding detergents
and using plastics such as polycarbonate
and Teflon that do not inhibit the growth
of bacterial cultures. These methods, which
have been referred to as high-throughput
extinction-culturing methods, led to the
isolation into pure culture of the most
important new heterotrophic marine strains
that have been cultured so far.
Other approaches to cultivation have used
microencapsulation techniques
11
, chambers
that allow the exchange of small molecules
with the environment
12
, floating filters
13,14
,
micromanipulation
15
or, simply, low-nutrient
agar plates
16
to cultivate novel microorgan-
isms. Although the details of these approaches
differ, they are all based on the same princi-
ples of re-creating the low-nutrient conditions
of natural environments and overcoming the
tendency of rapidly growing cells to over-
whelm species that divide less often. These
approaches have promise, as do traditional
enrichment strategies that target organisms
with unusual metabolisms
17
. Although
genomic information has not been a major
factor in the isolation of new marine organ-
isms, it has been exploited to design isolation
strategies for bacteria that are present in diff-
erent environments
18,19
, and it is only a matter
of time before genomic or metagenomic
information contributes to the isolation of a
marine bacterial or archaeal species.
Strains that represent many of the most
abundant marine clades have been isolated
into pure culture in recent years, but other
important clades still lack any cultured
representatives
20,21
(FIG. 2). Some of the uncul-
tured clades originate from phyla that are
associated with unusual metabolisms, which
suggests that their cultivation could depend
on successfully determining their ecological
niche. For example, the recent cultivation
of Nitrosopumilus maritimus SCM-1, which
was the first cultured representative of the
Group I Marine Crenarchaeota, succeeded
because of a specific strategy that excluded
bacteria with antibiotics and aimed to isolate
archaeal species that can oxidize ammonium
to yield energy
22
. The SAR202 clade, which
lacks cultured representatives, belongs to the
phylum Chloroflexi, which includes photo-
heterotrophs and anaerobes that have the
capacity to oxidize halogenated compounds.
The SAR202 clade is one of several that
have been relegated to regions that are just
below the euphotic zone
23
. Another important
group that lacks cultured representatives is
the SAR86 group of gammaproteobacteria,
which account for approximately 10% of
the total prokaryotic microbial community
in the ocean surface layer
24
. The discovery
of the light-driven, proton pump proteo-
rhodopsin in the fragmentary genome data
OPINION
The importance of culturing
bacterioplankton in the ‘omics’ age
Stephen Giovannoni and Ulrich Stingl
Abstract | Progress in the culturing of microorganisms that are important to ocean
ecology has recently accelerated, and technology has been a factor in these
advances. However, rather than a single technological breakthrough, a combination
of methods now enable microbiologists to screen large numbers of cultures and
manipulate cells that are growing at the low biomass densities that are
characteristic of those found in seawater. The value of ribosomal RNA databases
has been reaffirmed, as they provide nucleic-acid probes for screening to identify
important new species in culture. The new cultivation approaches have focused
on specific targets that ecological studies suggest are significant for geochemical
transformations, such as SAR11. Here, we review how to cultivate marine
oligotrophs and why it is worth the effort.
PERSPECTIVES
820 | OCTOBER 2007 | VOLUME 5 www.nature.com/reviews/micro
PERSPECTIVES
© 2007 Nature Publishing Group