Does the global microbiota consist of a few cosmopolitan species?
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Ecología Austral 16:85-90. Junio 2006
Asociación Argentina de Ecología
Debate
Does the global microbiota consist of a few cosmopolitan species?
RAMIRO E LOGARES
Limnology Div., Ecology Dept., Lund University, Lund, Sweden
[Keywords: cosmopolitanisms, endemics, microbes]
[Palabras clave: cosmopolitanismo, endémicos, microbios]
Biogeography studies the distribution of ryotes where sexual reproduction is known
biodiversity over space and time. Currently, (Andersen 1998). In a more controversial ap-
there is a strong debate on the biodiversity and proach, a group of researchers working on
biogeography of free-living microorganisms. prokaryotes have defined that organisms hav-
For several years, morphological studies have ing more than 70% of DNA-DNA similarity
promoted the idea that, at the global level, there belong to the same species (Wayne et al. 1987).
is a relatively small number of cosmopolitan
microbial species (Baas-Becking 1934; Finlay For years, the use of the MSC in microbial
2002, 2004; Fenchel 2005). This view has been taxonomy has promoted the view that the glo-
the most popular until recently, when molecu- bal microbiota consists of a relatively small
lar data started to unveil a much more com- number of cosmopolitan species; ‘the cosmo-
plex scenario. Within the realm of this contro- politan view’ (Finlay 2002, 2004). The most
versy, the objectives of this work are twofold: popular hypothesis for explaining this puta-
a) to review the traditional viewpoints on mi- tive pattern claims that due to their small sizes
crobial biodiversity and biogeography and, b) and huge abundances, microbes have no geo-
to present and discuss new molecular data graphical barriers for their dispersal (Fenchel
which are challenging previous ideas. 2005). As a consequence, there is little oppor-
tunity for genetic diversification and therefore,
Since the number of species relies on the cho- a low number of cosmopolitan species should
sen species definition, any discussion on bio- be expected. In agreement with these ideas,
diversity and biogeography needs to mention Griffin et al. (2002) indicate that between 1018
upon which species concept conclusions are and 1020 microorganisms are transported an-
based. So far, the Morphological Species Con- nually through the atmosphere, making it dif-
cept (MSC; species are groups of morphologi- ficult to imagine how topographic features of
cally identical or very similar organisms (Futu- the Earth’s surface could act as barriers for
yma 1998)) has been the most popular defini- their dispersal. Morphological studies support
tion in studies on microbial biodiversity and the ‘cosmopolitan hypothesis’ by indicating
biogeography. In a few cases, the Biological that there would be less than 5.000 species of
Species Concept (BSC; species are groups of microbes, a number quite low in comparison
interbreeding natural populations that are re- with the estimated 750.000 species of insects
productively isolated from other such groups or 280.000 of all other animals (Papke & Ward
(Mayr 1942)) has been applied to microeuka- 2004).
Limnology Div., Ecology Dept., Lund Univer-
sity. Sölvegatan 37 SE-223 62, Lund, Sweden. Recibido: 20 de octubre de 2004; Fin de arbitraje: 16 de mayo
Ramiro.Logares@limnol.lu.se de 2006; Aceptado: 16 de mayo de 200686 RE LOGARES Ecología Austral 16:85-90
A lack of biogeographic patterns and a low species are in fact composed of genetically di-
global diversity for free-living microbes has vergent populations or cryptic species. For in-
been the most accepted view until the advent stance, Montresor et al. (2003b) carried out
of molecular studies. Interestingly, some mo- morphological and genetic studies on differ-
lecular data support the ‘cosmopolitan hypoth- ent populations of the cosmopolitan marine
esis’ by showing a low genetic differentiation dinoflagellate Scrippsiella trochoidea and found
between populations separated by continen- that within the same morphotype, there are
tal distances (e.g. Darling et al. 2000; Montresor strains which show a genetic differentiation
et al. 2003a). However, there are mounting data that is in the order of what is normally found
revealing a very different picture, as it will be between other dinoflagellate species. In the
described and discussed in the following sec- light of their data, it seems likely that the
tions. morphotype known as Scrippsiella trochoidea
is actually a complex of cryptic species.
Is there a relatively low number of microbial
A good example of how similar morphologies
species?
can mask biodiversity comes from coccoid pico-
planktonic algae, which are mere tiny ( 99 % of microorganisms are
on other areas of the genome. Thus, it would not cultivable using standard techniques
not be surprising if it is revealed that several (Aman et al. 1995; Oren 2004). During the last
well established microbial species defined on decade, phylogenetic data from ribosomal
a morphological basis (morphospecies) are DNA (rDNA) sequences directly amplified
actually an agglomeration of a range of genetic from environmental samples (environmental
and physiological strains/species that are DNA surveys), revealed an unexpected diver-
morphologically undistinguishable. An in- sity of prokaryotes (Giovannoni et al. 1990;
creasing number of molecular studies are Fuhrman et al. 1992; Hugenholtz et al. 1998).
clearly pointing in this direction (e.g. Pace More recently, the same approach was used
1997; Potter et al. 1997; Daugbjerg et al. 2000; on marine microeukaryotes, revealing not only
Coleman 1996, 2001a, 2001b; Casamatta et al. an unsuspected high diversity, but also the
2003; Kim et al. 2004; Wilson et al. 2005). Alto- presence of several novel organisms with un-
gether, they are showing that several morpho- known close relatives (López-Garcia et al.
DebateJunio de 2006 MICROBIAL BIODIVERSITY AND BIOGEOGRAPHY 87 2001; Moreira & López-Garcia 2002). For in- lations of the hyperthermophilic prokaryote, stance, Moon-van der Staay et al. (2001) used Sulfolobus, are geographically isolated from one the environmental DNA approach to investi- another. In other words, thousands of kilome- gate the eukaryotic diversity in marine picoplank- ters of separation have left a genetic imprint in ton. They took one plankton sample (
88 RE LOGARES Ecología Austral 16:85-90
Geographical isolation has traditionally been To date, molecular techniques have been
regarded as the prevailing agent of microbial highly successful in the investigation of mi-
divergence (Papke & Ward 2004). However, crobial biodiversity and biogeography, but new
molecular data suggest that local adaptation studies including more taxa from different lo-
plays a significant role in microbial diversifi- cations are needed to gain a better understand-
cation (e.g. Rynearson & Armbrust 2000, 2004; ing of microbial diversification, biodiversity
Casamatta et al. 2003; Saez et al. 2003; Kim et and biogeography. It should always be remem-
al. 2004; Wilson et al. 2005; Coleman et al. bered that most of the diversity of life is micro-
2006; Johnson et al. 2006). The role of natural scopic, thus, studying microbial diversification
selection in the divergence and eventual spe- is necessary for understanding the process of
ciation of organisms in general has been re- evolution as a whole. There are also practical
cently reconsidered, receiving support from reasons for investigating microbial diversity
natural (Hendry et al. 2000; Rundle et al. 2000), and biogeography. For instance, in the search
laboratory (Rainey & Travisano 1998; Rainey for novel drugs or compounds of commercial
et al. 2000) and theoretical (Doebeli et al. 2005) importance as well as in the fight against mi-
studies. In particular, there is increasing evi-
crobial diseases (like malaria) and microbial
dence that natural selection can generate ex-
species that produce enormous economical
ceptionally rapid divergences, as illustrated
loses (e.g. dinoflagellates during blooms).
by the diverse macroorganisms that have colo-
nized islands or lakes (Orr & Smith 1998;
Coyne & Orr 2004). Evidence also indicates ACKNOWLEDGMENTS
that natural selection can generate rapid di-
vergences in microbes (Leblond et al. 2006;
Logares et al. 2006). Special thanks to K. Rengefors, L. A. Hansson
(Lund University) and J. Leblond (Middle Ten-
Molecular data indicate that microbial dis- nessee State University) for providing valuable
persal can be restricted by distance and/or comments and suggestions that helped to im-
geographical features (e.g. Wilkinson 2001; prove this manuscript. The Swedish Research
Whitaker et al. 2003; Martiny et al. 2006). Fol- Council and the SEED project contract, GOCE-
lowing the classical speciation theory, dis- CT-2005-003875 (European Commission Di-
persal restrictions will diminish gene flow be- rectorate General Research), to K. R. provided
tween populations, which will then further financial support.
diverge with time (by genetic drift and /or natu-
ral selection) to eventually form new strain/
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