Skip to main content
PMC home page
Astrobiology logoLink to Astrobiology
. 2012 Jul;12(7):634–640. doi: 10.1089/ast.2011.0768

Travel, Sex, and Food: What's Speciation Got to Do with It?

Valeria Souza 1,✉, Luis E Eguiarte 1, Michael Travisano 2, James J Elser 3, Christine Rooks 1, Janet L Siefert 4
PMCID: PMC3426884  PMID: 22920513

Abstract

We discuss the potential interactions among travel (dispersal and gene flow), bacterial “sex” (mainly as horizontal gene transfer), and food (metabolic plasticity and responses to nutrient availability) in shaping microbial communities. With regard to our work at a unique desert oasis, the Cuatro Ciénegas Basin in Coahuila, Mexico, we propose that diversification and low phosphorus availability, in combination with mechanisms for nutrient recycling and community cohesion, result in enhanced speciation through reproductive as well as geographic isolation. We also discuss these mechanisms in the broader sense of ecology and evolution. Of special relevance to astrobiology and central to evolutionary biology, we ask why there are so many species on Earth and provide a working hypothesis and a conceptual framework within which to consider the question. Key Words: Microbial ecology—Microbial mats—Evolution—Horizontal gene transfer—Metabolism. Astrobiology 12, 634–640.

1. Introduction

We now know that microbes interact with their environment in ways that can be described in terms of biogeographic regions (Hanson et al., 2012) that can house not only cosmopolitan species but also microorganisms that are endemic and/or specific to a particular ecology. It is the individuality of this latter group that largely characterizes a specific biogeographic region or regions. This characterization provides an empirical and theoretical framework in which to consider the processes and mechanisms of a microbial population adapting to its local environment independently of its taxonomical status. The ability to describe biogeographic regions is completely tied to our increased technical proficiency in sequencing target nucleic acids at a large scale in environmental samples, which allows us to move from considering microbial ecology in single, pure, environmentally derived culture analysis to studies of whole communities across geographic distance. This is precisely what microbial population geneticists needed to begin to consider the population dynamics of microbes. Indeed, the call is to bear in mind classic evolutionary processes—selection, drift, dispersal, and mutation—as the mechanisms that maintain microbial biogeographic patterns (Hanson et al., 2012).

However, our ability to assess biogeographic regions provides another opportunity for exploration to discover the actual processes that serve to populate a biogeographic region with its species. In other words, which mechanisms create, maintain, or diminish diversity in a biogeographic region? This specific question is part of a larger scientific quest: understanding the maintenance of global diversity. Certainly it is this diversity that fuels the fundamental, underlying processes that maintain the Earth system in terms of elemental recycling, as well as life's dynamic and tenacious ability to colonize an astonishing array of habitats. It even fuels our intelligent speculation for extraterrestrial life.

The Cuatro Ciénegas Basin (CCB) is a unique, well-studied biogeographic region, an oasis in the Chihuahuan Desert with very little nutrients (ultraoligotrophic) and a high biodiversity (Souza et al., 2006, 2008). The widespread oligotrophy and geochemical conditions that impact the concentrations and relative ratios of limiting nutrient supplies (Elser et al., 2005) have resulted in utilization of the CCB as a research proxy for early Earth, when nutrients were extremely scarce (Anbar et al., 2007; Papineau, 2010), and as an analogue of Gale Crater on Mars, the current target of choice for exploration for NASA's Mars Science Laboratory.

Evidence from comparative genomics and molecular clock assessments from the CCB indicate that roughly 50% of the microbial taxa appear to be most closely related to other marine biogeographic regions rather than to microbes from inland waters. The most plausible explanation for this apparent genetic relict of a marine life is the geographic evidence for previous ancient oceans that entered the region 200 million years ago (Alcaraz et al., 2008, 2010; Desnues et al., 2008; Moreno-Letelier et al., 2011, 2012 in this issue; Peimbert et al., 2012 in this issue). However, molecular clock estimation places some of the constituents of the CCB to a divergence event in the Precambrian 800 million years ago (Domínguez-Escobar et al., 2011; Moreno-Letelier et al., 2011) with subsequent colonization in the area as well as with a consistent and ongoing local speciation and diversification in the microbial community, including viruses (Desnues et al., 2008), bacteria (Escalante et al., 2008, 2009; Cerritos et al., 2011; Rebollar et al., 2012), and diatoms (Winsborough et al., 2009). Thus, a significant portion of the CCB microbiota appears to have evolved from these relict ancestral marine taxa to form the extant and continuously diversifying local biota that defines a highly endemic CCB biogeographic region.

Here, we consider several factors that may have led to this apparent wealth of microbial diversity, with particular attention to the roles of travel (dispersal and gene flow), bacterial “sex” [both recombination within species and horizontal gene transfer (HGT) among lineages, as mediated by nutrient deficiency], and food (metabolic plasticity and responses to nutrient availability) in shaping microbial communities. Our motivation is to offer an additional conceptual framework for population microbiologists that can help progress our understanding of how diversity might be achieved and maintained in a biogeographic region. We do so in the context of the CCB, where genetic and geographic isolation of microorganisms has been observed under the constant pressure of an insufficient “food source.” Our working hypothesis (Souza et al., 2008) is that the extreme long-term oligotrophy has impacted the biogeographic region in such a way that populations have been isolated in their potential to access genetic resources through sex (HGT), which has promoted localized diversification with accompanying unusual rates of speciation.

2. Travel

The aquatic ecosystems of the CCB are located ca. 720 m above sea level and are separated from the closest shoreline by >800 km of mountainous and arid terrain. Although this effectively “isolates” these aquatic ecosystems from the closest marine environment, the possibility of long-range dispersal as a means of “seeding” these remote habitats must be excluded. As mentioned above, the idea of biogeographic regions in the microbial realm has been established recently. In contrast to macroorganisms, where it has been known for some time that distinct biogeographic patterns are the rule (Rosenzweig, 1995), the hypothesis that “everything is everywhere, but the environment selects” (EEBES, Baas Becking, 1934; de Wit and Bouvier 2006) has been the working rule of thumb for the microbial realm. Historically, the logic suggested that the combined effects of small body size, rapid asexual reproduction, and high population densities should facilitate broad, unlimited dispersal, which would prevent the formation of distinct microbial communities by distance and elimination of “detectable” biogeographic patterns (reviewed in Fenchel et al., 1997; Finlay and Clarke, 1999; Finlay, 2002; A.C. Martiny et al., 2006; Fierer, 2008; Cermeno and Falkowski, 2009; Shurin et al., 2009). Assessing EEBES has been difficult because less than 1% of the microbes can be cultured (Amann et al., 1995), and previous work may have overemphasized cosmopolitan generalists that are easy to culture. However, microbial ecologists are now deploying “cultivation independent” techniques, such as small-subunit 16S (ribosomal) rRNA gene analysis, to identify uncultivable microorganisms (Stackebrandt and Ebers, 2006), which allows for comprehensive assessment of EEBES for the first time.

Several methodologies have been employed to assess the diversification and species content of a biogeographic region with use of the 16S as a taxonomical marker, including phylogenetic reconstructions within individual species (Achtman et al., 1999; Helgason, et al., 2004) and community-level dynamics (Horner-Devine et al., 2004). Rarefaction curves (taxa-accumulation curves), whereby the number of operational taxonomic units (OTUs) are plotted as a function of sampling effort, rarely reach an asymptote (Curtis et al., 2002; Curtis and Sloan, 2005), even if hundreds of thousands of sequences are analyzed with next-generation methods such as 454 pyrosequencing tags (Sogin et al., 2006; Roesch et al., 2007; Fierer, 2008). At present, capturing the “full” genetic diversity within any given environmental sample appears to be extremely unlikely (Hughes et al., 2001; Curtis and Sloan, 2005), and this has led to the idea of chronic subsampling of the environment. If this is the case, we could easily imagine that each sampling site will have all the known taxa, and as a result we would expect little variation in the general microbial diversity as a function of distance, since each similar site would contain an equivalent list of taxa (Finlay, 2002). However, an increasing number of studies clearly indicate a positive power-law relationship between the number of species and the size of the area, which suggests both geographic structure and a particular accompanying community structure (Finlay, 2002, Torsvik et al., 2002; Papke et al., 2003; Whitaker et al., 2003; Horner-Devine et al., 2004; Gans et al., 2005; Noguez et al., 2005; Tringe et al., 2005; Silva et al., 2005; Hong et al., 2006; J.B.H. Martiny et al., 2006; Cadillo-Quiroz et al., 2012; Hanson et al., 2012).

Even if we can never be sure that our lack of sampling is missing a relevant part of the local diversity, common sense dictates that limits to global dispersal are numerous. Certainly, anaerobes would be a classic example of physiological limits on dispersal (Maron et al., 2005; Litchman, 2010). Even in the case of spore-forming generalists that can migrate effectively, such as Bacillus, some species within this genus exhibit considerable local differentiation and diversification (Stach et al., 2003; Alcaraz et al., 2008; Hubert et al., 2009; Jungblut et al., 2010; Oakley et al., 2010), which suggests limits to migration. A particular, good context within which to consider EEBES would be globally distributed but environmentally stringent environments. Recognizing that if EEBES is the mechanism most at play, such environments would select from the global pool; thus similar environments around the world should harbor the same organisms. Evidence suggests that this is at least partially true but only at relatively high taxonomic levels. For example, the genus Sulfolobus is located almost wherever there is volcanic activity, and S. solfataricus has been found in areas including Yellowstone National Park, Mount St. Helens, Iceland, Italy, and Russia (Brock et al., 1972). Nevertheless, population genetics has shown that geographic structure and differentiation of genotypes between sites are commonplace in Sulfolobus (Papke et al., 2003; Whitaker et al., 2003; Whitaker, 2006). Furthermore, a recent study in which high-throughput sequencing and comparative genomic tools were used shows clear patterns of differentiation between sites, while gene flow between coexisting isolates within a site ensures species cohesion at the local level (Cadillo-Quiroz et al., 2012). Greater efficiency in sampling techniques elsewhere provides similar results; geographic structure has been demonstrated in Desulfolobus (Oakley et al., 2010), deep-sea methanogens (Tavormina et al., 2010), Antarctic cyanobacteria (Pointing et al., 2009), and the marine Cyanobacteria Prochlorococcus (A.C. Martiny et al., 2006). This implies that even large-scale and intensive mixing via ocean currents does not obscure biogeographic patterns, even among microorganisms that were previously assumed to be cosmopolitan (Shapiro et al., 2012).

We see clear patterns of biogeographic regions with respect to the CCB. The geographic isolation occurs at small scales and, as a result and despite higher-level similarities (i.e., similar marine-related taxa), each site is different at increasing resolution from the other sampled sites (Desnues et al., 2008; Breitbart et al., 2009; Escalante et al., 2009; Bonilla-Rosso et al., 2012 in this issue; Rebollar et al., 2012). In fact, in the CCB we observe an increase in both gamma and beta diversity (the slope in the taxa-area power function) as we increase the sampling area. In contrast, a strong dominance of just a few taxa over large areas has been observed in other desert environments by researchers working with different methods at various sites (Kuske et al., 1997; Dunbar et al., 1999; Gundlapally and Garcia-Pichel, 2006).

In addition to evidence of geographic structure within the CCB, our findings suggest high local diversity, which appears to be independent of the sampling method (Souza et al., 2006; Escalante et al., 2008). Early studies revealed a higher number of OTUs of Bacillus than would generally be expected in an oligotrophic aquatic ecosystem. This included surveys of cultivated strains with the use of BOX-PCR and 16S rDNA gene sequences (Cerritos et al., 2011; G. Olmedo, personal communication). These studies revealed the presence of several new Bacillus species (Cerritos et al., 2008; M. Avitia and R. Cerritos, personal communication) with highly distinct genomes (Alcaraz et al., 2008, 2010).

These early hints have been borne out with more intensive work with next-generation genomics techniques. Recently, high-throughput sequencing of microbialites within the CCB, with 454 pyrosequencing and detailed metagenomic analysis, allowed for identification of 1200 unique OTUs in a single microbial mat, with very little overlap to other studied metagenomes from the CCB (Bonilla-Rosso et al., 2012 in this issue). Furthermore, with 454 pyrosequencing of 16S rDNA gene tags, 56,000 new OTUs were estimated in a single soil sample of the CCB, most of them different from another soil sample 1 km away (López-Lozano et al., personal communication). Considering that, with the same technique and the same primer, Sogin and co-authors (2006) found between 2000 and 3000 different OTUs in several marine sediment samples and remarked about the high diversity of this “rare biosphere,” Cuatro Ciénegas appears to be 10-fold more diverse. Paradoxically, this diversity is comparable with studies in fertile temperate soils, where the availability of organic matter is abundant and conditions are extremely humid (Curtis and Sloan, 2005; Fierer and Jackson, 2006; Roesch et al., 2007). However, the ample availability of resources, in community theory, can easily sustain a diverse community; it is the case of CCB biodiversity in extreme oligotrophy that is hard to explain. The fact that each sampling site is different from the next site suggests that either migration is rare or each community is adapted to very specific local conditions.

3. Sex

Prokaryotes reproduce by binary fission, which forms clonal lineages that diversify by mutations that slowly accumulate by vertical descent. This eventually gives rise to diversifying lineages, as new mutations steadily increase and new niches become available. Nevertheless, novel genetic variation is occasionally introduced by HGT, a form of bacterial sex. (In the microbial context, “sex” is considered the exchange of exogenous genetic material.) This input of new genes can arrive by plasmid acquisition (Anderson and Hughes, 2010) via double-stranded recombination, which is essentially mediated by proteins responsible for DNA repair. This is considered the main physical process by which genes are transferred between microbial donors and receptors in transduction (virus infection), transformation (DNA uptake by competent bacteria), or conjugation (plasmid dynamics) (Kuzminov, 1995; Seigneur et al., 1998; Cox, 2000; Redfield, 2001). A legacy of HGT is the potential for trait-based evolutionary innovations (Redfield, 2001). Depending on the genes that are mobilized and the ecological context of the receiver, HGT can have a strong adaptive value if it allows the acquiring cell to use new resources and occupy new niches (Bolhuis et al., 2010). For example, this is apparent with respect to the small, photosynthetic cyanobacterium Prochlorococcus, where each strain seems to possess a different strategy for scavenging P in the oligotrophic ocean gyres (A.C. Martiny et al., 2006). The patchwork pattern of their P acquisition genes, and evidence of viral components in their genomes, suggests that transduction by viruses is the mechanism for frequent HGT in these ocean dwellers (A.C. Martiny et al., 2006).

The notion of bacterial “sex” as a promiscuous senseless exchange of genes between different phyla was elegantly argued in the work of Ford Doolittle (Bapteste et al., 2008) and Howard Ochman (van Passel et al., 2008). This has led some researchers to claim that there are no bacterial species but merely the existence of a diverse pool of disposable genes (Lawrence and Retchless, 2010). This view is extreme, but it occurs in the context of a large effective population size where even rare migration of genes can have a large homogenizing effect (i.e., enteric bacteria) (Charlesworth and Charlesworth, 2010). If extensive bacterial sex is combined with the potential for limitless dispersal (via vectors such as plants and animals or atmospheric or ocean currents), the migration of genes, as well as cell-cell contact between individuals, could mix different populations. Consequently, this would result in the maintenance of a single cohesive gene pool and therefore reduce the probability of local differentiation. In the extreme version of this view of life, we cannot explain microbial diversity.

Despite the theoretical possibility of unlimited HGT, it has been argued that the effects of bacterial “sex” are, in fact, exaggerated. For example, a reduced role for HGT may reflect inherent differences in overall cell organization between lineages, which would significantly lower the success of recombinants resulting from lateral gene exchange (see review by Thomas and Nielsen, 2005). Furthermore, lateral gene exchange occurs rarely between different lineages, even if it may have important consequences for population structure within species (e.g., Souza et al., 1992, 1997; Silva et al., 2003, 2005; Castillo et al., 2005). For example, we believe that the case of antibiotic resistance moving rampantly between microbes in hospitals represents an extreme case of positive selection between extremely stressed pathogens. Such pathogens may exchange plasmids with integrons but nevertheless maintain an intact genetic core (see review by Anderson and Hughes, 2010). Consequently, this effectively dispels the notion of a large pool of available genes; therefore, it is possible to identify lineages and, hence, species.

The CCB is a remarkable case of microbial endemism that is the product of verifiable events of HGT, as demonstrated by the genome of Bacillus coahuilensis (Alcaraz et al., 2008). In general, members of the genus Bacillus are understood to be cosmopolitan travelers that are capable of broad dispersal owing to their ability to form spores; therefore, they have the capacity to endure periods of environmental instability (Porwal et al., 2009). The genome of B. coahuilensis, however, suggests the evolution of unique adaptations to a chronically low P environment, including the remarkable ability to produce sulfolipids in place of P-rich phospholipids and significant reductions in genome size (Alcaraz et al., 2008). Both of these adaptations may be interpreted as P-sparing mechanisms that reduce the overall cell demand for phosphate (Lewis, 1985; Alcaraz et al., 2008; Souza et al., 2008). Such specialization could also suggest that this particular species is a long-term resident of the CCB and does not travel well; it carries few of the spore-forming genes known for B. subtilis, and interestingly, the same occurs with other species of Bacillus within the CCB (Alcaraz et al., 2010). Furthermore, Bacillus from the CCB seems to sporulate at low frequency (G. Olmedo, personal communication). If such evolutionary “fine-tuning” is required by the majority of microorganisms that inhabit the CCB, then colonization by invading bacteria is unlikely not only because any new arrival will fail to outcompete the established cohesive microbial community (Litchman, 2010) but also these newcomers may become a likely source of nutrients for local scavengers that present mechanisms for bursting nonresistant cells (Peimbert et al., 2012).

4. Food

As mentioned before, CCB communities are severely limited by phosphorus, and this has effects on trophic interactions (Elser et al., 2005, 2006). CCB waters have low levels of available phosphorus together with a strong stoichiometric imbalance relative to N. In this case, it appears that species diversity is maintained in the face of fierce competition for dwindling resources, which places a premium on the ability to scavenge for phosphorus. Metagenomic analysis of an oncolite within a ultraoligotrophic river in the CCB [Río Mesquites (C:N:P of 900:150:1; Breitbart et al., 2009)] implied that even though the microbial community was dominated by Cyanobacteria, there was a high number of ribotypes (261 ribotypes) within this phylum. As expected, high-affinity phosphorus acquisition genes from the pho and pst gene families were overrepresented in this metagenome (Breitbart et al., 2009), which supports the concept of specialization to an extremely P-limited environment. Conditions experienced by the microbes in these Río Mesquites oncolites, which move with the oxygen-rich river flow, are totally different from those experienced in the Pozas Rojas in the CCB, where stationary hypersaline microbial mats experience highly variable temperature (seasonal temperature 4–75°C) and the probabilities of colonization of new niches are reduced. While oligotrophy and extreme stoichiometric imbalance is a shared condition for these two sites (N:P ratios at Pozas Rojas are potentially as imbalanced as 157:1), a metagenome of Poza Roja points toward alternative strategies, as genes affiliated with phosphorus metabolism are not overrepresented in this community. Here, gene composition suggests that an alternative strategy of partitioning or “micro-splitting” the niche by extreme specialization in degradation of an ample and complex array of metabolic by-products (Peimbert et al., 2012 in this issue). As a result of this fierce competition, in this community we observed 355 different ribotypes of novel Pseudomonas in addition to 20 more phyla, including Cyanobacteria, Chlorobium, and Chloroflexi as primary producers (Bonilla-Rosso et al., 2012 in this issue). Concomitantly, the presence of several genes for antibiotic production and resistance implies that the Pseudomonas in Pozas Rojas may be evolving in order to escape antagonistic and competitive interactions. This is in line with a “Red Queen” model (Venditti et al., 2010; Wilson and Sherman, 2010), whereby species constantly arise by reproductive isolation and rare stochastic events.

We suggest that the microbial diversity of the CCB is maintained by the mechanisms that include lack of food (metabolic plasticity in response to nutrient availability), HGT (relevant but infrequent), and ineffective travel (isolation) due to both the low genetic diversity in the local clones and the fierce competition for scarce nutrients. The combination of diversification and low-P conditions, together with mechanisms for phosphorous acquisition in extant CCB bacteria, were the impetus for our working hypothesis. More explicitly, the lack of P results in reduced HGT because of reduced cell-to-cell contact under oligotrophy, high rates of degradation of free DNA in the environment, and muted viral reproduction (Souza et al., 2008). Stated simply, low P enhances speciation by promoting both geographic and reproductive isolation. However, beyond the specific case of the CCB, we suggest that, to study the occurrence and origin of endemic communities comprehensively, not only must diversity be addressed but the mechanisms that generate and maintain it must be assessed as well. In general, we strongly suggest that those studies should be accompanied with detailed studies of the ecological conditions of the site as well as their geological history.

5. Conclusions and Future Work

Relative to “complex” eukaryotic life, prokaryotes collectively possess an enormous metabolic diversity due to their deep evolutionary roots and remarkable capacity to adapt and ultimately thrive even under some of the most inhospitable conditions on Earth. When we consider the evolutionary causes that have facilitated Earth's biogeochemical stability and enormous diversity, the role of “travel, sex, and food” appears to be crucial. To assess this, not only do we need to explore other analogues of early Earth where food is scarce but we should also experimentally manipulate nutrient availability in microbial communities at places like the CCB and monitor how microbial diversity responds to shifts in nutrients, either via studies of well-studied focal taxa such as Pseudomonads or Bacilli or via inference by using metagenomics and transcriptomics. Such experiments are already underway at the CCB, where we are also embarking on studies in which open-air mesocosms within pools of different sizes are being used and targeting a diverse array of species to see, with the use of clone libraries, how migrants are accepted, or not, into microbial communities. With such studies in this “desert Galapagos,” we hope to further illuminate the enduring puzzle of Earth's remarkable microbial diversity.

Acknowledgments

This work was completed by Valeria Souza and Luis E. Eguiarte during their sabbatical leave in UCI. Funding for this project was provided by a DGAPA/UNAM scholarship to Valeria Souza and UC-Mexus to Luis E. Eguiarte. The data that prompted these ideas were supported by grants from NASA and NSF to James J. Elser and Valeria Souza, CONACyT-FONSEC SEMARNAT 2006-C01-23459, CONACYT-SEP 50507, and WWF-Alianza Fundación Carlos Slim to V.S. We are truly thankful for the invaluable insights of Dr. Wim van der Putten and of our collaborator Gabriela Olmedo.

Abbreviations

CCB, Cuatro Ciénegas Basin; EEBES, “everything is everywhere, but the environment selects”; HGT, horizontal gene transfer; OTUs, operational taxonomic units.

References

  1. Achtman M. Azuma T. Berg D.E. Ito Y. Morelli G. Pan Z.J. Suerbaum S. Thompson S.A. Van Der Ende A. Van Doorn L.J. Recombination and clonal groupings within Helicobacter pylori from different geographical regions. Mol Microbiol. 1999;32:459–470. doi: 10.1046/j.1365-2958.1999.01382.x. [DOI] [PubMed] [Google Scholar]
  2. Alcaraz L.D. Olmedo G. Bonilla G. Cerritos R. Hernández G. Cruz A. Ramírez E. Putonti C. Jiménez B. Martínez E. López V. Arvizu J.L. Ayala F. Razo F. Caballero J. Siefert J. Eguiarte L. Vielle J.P. Martínez O. Souza V. Herrera-Estrella A. Herrera-Estrella L. The genome of Bacillus coahuilensis reveals adaptations essential for survival in the relic of an ancient marine environment. Proc Natl Acad Sci USA. 2008;105:5803–5808. doi: 10.1073/pnas.0800981105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Alcaraz L.D. Moreno-Hagelsieb G. Eguiarte L.E. Souza V. Herrera-Estrella L. Olmedo G. Understanding the evolutionary relationships and major traits of Bacillus through comparative genomics. BMC Genomics. 2010;11:332. doi: 10.1186/1471-2164-11-332. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Amann R.I. Ludwig W. Schleifer K.H. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev. 1995;59:143–169. doi: 10.1128/mr.59.1.143-169.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Anbar A.D. Duan Y. Lyons T.M. Arnold G.L. Kendall B. Creaser R.A. Kaufman A.J. Gordon G.W. Scott C. Garvin J. Buick R. A whiff of oxygen before the Great Oxidation Event? Science. 2007;317:1903–1906. doi: 10.1126/science.1140325. [DOI] [PubMed] [Google Scholar]
  6. Anderson D.I. Hughes D. Antibiotic resistance and its cost: is it possible to reverse resistance? Nat Rev Microbiol. 2010;8:260–271. doi: 10.1038/nrmicro2319. [DOI] [PubMed] [Google Scholar]
  7. Baas Becking L. Geobiologie of inleiding tot de milieukunde. Van Stockum & Zoon, The Hague; the Netherlands: 1934. [Google Scholar]
  8. Bapteste E. Susko E. Leigh J. Ruiz-Trillo I. Bucknam J. Doolittle W.F. Alternative methods for concatenation of core genes indicate a lack of resolution in deep nodes of the prokaryotic phylogeny. Mol Biol Evol. 2008;25:83–91. doi: 10.1093/molbev/msm229. [DOI] [PubMed] [Google Scholar]
  9. Bolhuis H. Severin I. Confurius-Guns V. Wollenzien U.I.A. Stal L.J. Horizontal transfer of the nitrogen fixation gene cluster in the cyanobacterium Microcoleus chthonoplastes. ISME J. 2010;4:121–130. doi: 10.1038/ismej.2009.99. [DOI] [PubMed] [Google Scholar]
  10. Bonilla-Rosso G. Peimbert M. Alcaraz L.D. Hernández I. Eguiarte L.E. Olmedo-Alvarez G. Souza V. Comparative metagenomics of two microbial mats at Cuatro Ciénegas Basin II: community structure and composition in oligotrophic environments. Astrobiology. 2012;12:659–673. doi: 10.1089/ast.2011.0724. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Breitbart M. Hoare A. Nitti A. Siefert J. Haynes M. Dinsdale E. Edwards R. Souza V. Rohwer F. Hollander D. Metagenomic and stable isotopic analyses of modern freshwater microbialites in Cuatro Cienegas, Mexico. Environ Microbiol. 2009;11:16–34. doi: 10.1111/j.1462-2920.2008.01725.x. [DOI] [PubMed] [Google Scholar]
  12. Brock T.D. Brock K.M. Belly R.T. Weiss R.L. Sulfolobus: a new genus of sulfur-oxidizing bacteria living at low pH and high temperature. Arch Mikrobiol. 1972;84:54–68. doi: 10.1007/BF00408082. [DOI] [PubMed] [Google Scholar]
  13. Cadillo-Quiroz H. Didelot X. Held N.L. Herrera A. Darling A. Reno M.L. Krause D.J. Whitaker R.J. Patterns of gene flow define species thermophilic Archaea. PLoS Biol. 2012;10:e10011265. doi: 10.1371/journal.pbio.1001265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Castillo-Cobián A. Eguiarte L.E. Souza V. A genomic population genetics analysis of the pathogenic LEE island in E. coli: in search of the unit of selection. Proc Natl Acad Sci USA. 2005;102:1542–1547. doi: 10.1073/pnas.0408633102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Cermeno P. Falkowski P.G. Controls on diatom biogeography in the ocean. Science. 2009;325:1539–1541. doi: 10.1126/science.1174159. [DOI] [PubMed] [Google Scholar]
  16. Cerritos R. Vinuesa P. Eguiarte L.E. Herrera-Estrella L. Alcaraz-Peraza L.D. Arvizu-Gomez J.L. Olmedo G. Ramirez E. Siefert J.L. Souza V. Bacillus coahuilensis sp. nov., a moderately halophilic species from a desiccation lagoon in the Cuatro Cienegas Valley in Coahuila, Mexico. Int J Syst Evol Microbiol. 2008;58:919–923. doi: 10.1099/ijs.0.64959-0. [DOI] [PubMed] [Google Scholar]
  17. Cerritos R. Eguiarte L.E. Avitia M. Siefert J. Travisano M. Rodríguez-Verdugo A. Souza V. Diversity of culturable thermo-resistant aquatic bacteria along an environmental gradient in Cuatro Ciénegas, Coahuila, México. Antonie van Leeuwenhoek. 2011;99:303–318. doi: 10.1007/s10482-010-9490-9. [DOI] [PubMed] [Google Scholar]
  18. Charlesworth B. Charlesworth D. Elements of Evolutionary Genetics. Roberts & Co. Publishers; Greenwood Village, CO: 2010. [Google Scholar]
  19. Cox M.M. Recombinational DNA repair in bacteria and the RecA protein. Prog Nucleic Acid Res Mol Biol. 2000;63:311–366. doi: 10.1016/s0079-6603(08)60726-6. [DOI] [PubMed] [Google Scholar]
  20. Curtis T.P. Sloan W.T. Exploring microbial diversity—a vast below. Science. 2005;309:1331–1333. doi: 10.1126/science.1118176. [DOI] [PubMed] [Google Scholar]
  21. Curtis T.P. Sloan W.T. Scannell J.W. Estimating prokaryotic diversity and its limits. Proc Natl Acad Sci USA. 2002;99:10494–10499. doi: 10.1073/pnas.142680199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. de Wit R. Bouvier T. ‘Everything is everywhere, but, the environment selects’: what did Baas Becking and Beijerinck really say? Environ Microbiol. 2006;8:755–758. doi: 10.1111/j.1462-2920.2006.01017.x. [DOI] [PubMed] [Google Scholar]
  23. Desnues C. Rodriguez-Brito B. Rayhawk S. Kelley S. Tran T. Haynes M. Liu H. Furlan M. Wegley L. Chau B. Ruan Y. Hall D. Angly F.E. Edwards R.A. Li L. Thurber R.V. Reid R.P. Siefert J. Souza V. Valentine D.L. Swan B.K. Breitbart M. Rohwer F. Biodiversity and biogeography of phages in modern stromatolites and thrombolites. Nature. 2008;452:340–343. doi: 10.1038/nature06735. [DOI] [PubMed] [Google Scholar]
  24. Domínguez-Escobar J. Beltrán Y. Bergman B. Díez B. Ininbergs K. Souza V. Falcón L.F. Phylogenetic and molecular clock inferences of cyanobacterial strains within Rivulariaceae from distant environments. FEMS Microbiol Lett. 2011;316:90–99. doi: 10.1111/j.1574-6968.2010.02195.x. [DOI] [PubMed] [Google Scholar]
  25. Dunbar J. Takala S. Barns S.M. Davis J.A. Kuske C.R. Levels of bacterial community diversity in four arid soils compared by cultivation and 16S rRNA gene cloning. Appl Environ Microbiol. 1999;65:1662–1669. doi: 10.1128/aem.65.4.1662-1669.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Elser J.J. Schampel J.H. Garcia-Pichel F. Wade B.D. Souza V. Eguiarte L. Escalante A.E. Farmer J.D. Effects of phosphorus enrichment and grazing snails on modern stromatolitic microbial communities. Freshw Biol. 2005;50:1808–1825. [Google Scholar]
  27. Elser J.J. Watts J. Schampel J.H. Farmer J.D. Early food webs on a trophic knife-edge? Experimental data from a modern microbialite-based ecosystem. Ecol Lett. 2006;9:295–303. doi: 10.1111/j.1461-0248.2005.00873.x. [DOI] [PubMed] [Google Scholar]
  28. Escalante A.E. Eguiarte L.E. Espinosa-Asuar L. Forney L.J. Noguez A.M. Saldivar V.S. Diversity of aquatic prokaryotic communities in the Cuatro Cienegas Basin. FEMS Microbiol Ecol. 2008;65:50–60. doi: 10.1111/j.1574-6941.2008.00496.x. [DOI] [PubMed] [Google Scholar]
  29. Escalante A.E. Caballero-Mellado J. Martinez-Aguilar L. Rodriguez-Verdugo A. Gonzalez-Gonzalez A. Toribio-Jimenez J. Souza V. Pseudomonas cuatrocienegasensis sp nov., isolated from an evaporating lagoon in the Cuatro Cienegas valley in Coahuila, Mexico. Int J Syst Evol Microbiol. 2009;59:1416–1420. doi: 10.1099/ijs.0.006189-0. [DOI] [PubMed] [Google Scholar]
  30. Fenchel T. Esteban G.F. Finlay B.J. Local versus global diversity of microorganisms: cryptic diversity of ciliated protozoa. Oikos. 1997;80:220–225. [Google Scholar]
  31. Fierer N. Microbial biogeography: patterns in microbial diversity across space and time. In: Zengler K., editor. Accessing Uncultivated Microorganisms: From the Environment to Organisms and Genomes and Back. ASM Press; Washington DC: 2008. pp. 95–115. [Google Scholar]
  32. Fierer N. Jackson R.B. The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci USA. 2006;103:626–631. doi: 10.1073/pnas.0507535103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Finlay B.J. Global dispersal of free-living microbial eukaryote species. Science. 2002;296:1061–1063. doi: 10.1126/science.1070710. [DOI] [PubMed] [Google Scholar]
  34. Finlay B.J. Clarke K.J. Ubiquitous dispersal of microbial species. Nature. 1999;400:828. [Google Scholar]
  35. Gans J. Wolinsky M. Dunbar J. Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science. 2005;309:1387–1390. doi: 10.1126/science.1112665. [DOI] [PubMed] [Google Scholar]
  36. Gundlapally S.R. Garcia-Pichel F. The community and phylogenetic diversity of biological soil crusts in the Colorado Plateau studied by molecular fingerprinting and intensive cultivation. Microb Ecol. 2006;52:345–357. doi: 10.1007/s00248-006-9011-6. [DOI] [PubMed] [Google Scholar]
  37. Hanson Ch.A. Fuhrman J.A. Horner-Devine M.C. Martiny J.B.H. Beyond biogeographic patterns: processes shaping the microbial landscape. Nat Rev Microbiol. 2012;10:497–506. doi: 10.1038/nrmicro2795. [DOI] [PubMed] [Google Scholar]
  38. Helgason E. Tourasse N.J. Meisal R. Caugant D.A. Kolstø A.B. Multilocus sequence typing scheme for bacteria of the Bacillus cereus group. Appl Environ Microbiol. 2004;70:191–201. doi: 10.1128/AEM.70.1.191-201.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Hong S.H. Bunge J. Jeon S.O. Epstein S.S. Predicting microbial species richness. Proc Natl Acad Sci USA. 2006;103:117–122. doi: 10.1073/pnas.0507245102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Horner-Devine M.C. Lage M. Hughes J.B. Bohannan B.J.M. A taxa-area relationship for bacteria. Nature. 2004;432:750–753. doi: 10.1038/nature03073. [DOI] [PubMed] [Google Scholar]
  41. Hubert C. Loy A. Nickel M. Arnosti C. Baranyi C. Brüchert V. Ferdelman T. Finster K. Christensen F.M. Rosa de Rezende J. Vandieken V. Jørgensen B.B. A constant flux of diverse thermophilic bacteria into the cold Arctic seabed. Science. 2009;325:1541–1544. doi: 10.1126/science.1174012. [DOI] [PubMed] [Google Scholar]
  42. Hughes J.B. Hellmann J.J. Ricketts T.H. Bohannan B.J.M. Counting the uncountable: statistical approaches to estimating microbial diversity. Appl Environ Microbiol. 2001;67:4399–4406. doi: 10.1128/AEM.67.10.4399-4406.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Jungblut A.D. Lovejoy C. Vincent W.F. Global distribution of cyanobacterial ecotypes in the cold biosphere. ISME J. 2010;4:191–202. doi: 10.1038/ismej.2009.113. [DOI] [PubMed] [Google Scholar]
  44. Kuske C.R. Barns S.M. Busch J.D. Diverse uncultivated bacterial groups from soils of the arid southwestern United States that are present in many geographic regions. Appl Environ Microbiol. 1997;63:3614–3621. doi: 10.1128/aem.63.9.3614-3621.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Kuzminov A. Collapse and repair of replication forks in Escherichia coli. Mol Microbiol. 1995;16:373–384. doi: 10.1111/j.1365-2958.1995.tb02403.x. [DOI] [PubMed] [Google Scholar]
  46. Lawrence J.G. Retchless A.C. The myth of bacterial species and speciation. Biol Philos. 2010;25:569–588. [Google Scholar]
  47. Lewis W.M. Nutrient scarcity as an evolutionary cause of haploidy. Am Nat. 1985;125:692–701. [Google Scholar]
  48. Litchman E. Invisible invaders: non-pathogenic invasive microbes in aquatic and terrestrial ecosystems. Ecol Lett. 2010;13:1560–1572. doi: 10.1111/j.1461-0248.2010.01544.x. [DOI] [PubMed] [Google Scholar]
  49. Maron P.A. Lejon D.P.H. Carvalho E. Bizet K. Lemanceau P. Ranjard L. Mougel C. Assessing genetic structure and diversity of airborne bacterial communities by DNA fingerprinting and 16S rDNA clone library. Atmos Environ. 2005;39:3687–3695. [Google Scholar]
  50. Martiny A.C. Coleman M.L. Chisholm S.W. Phosphate acquisition genes in Prochlorococcus ecotypes: evidence for genome-wide adaptation. Proc Natl Acad Sci USA. 2006;103:12552–12557. doi: 10.1073/pnas.0601301103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Martiny J.B.H. Bohannan B.J.M. Brown J.H. Colwell R.K. Fuhrman J.A. Green J.L. Horner-Devine M.C. Kane M. Krumins J.A. Kuske C.R. Morin P.J. Naeem S. Ovreås L. Reysenbach A.L. Smith V.H. Staley J.T. Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol. 2006;4:102–112. doi: 10.1038/nrmicro1341. [DOI] [PubMed] [Google Scholar]
  52. Moreno-Letelier A. Olmedo G. Eguiarte L.E. Martínez-Castilla L. Souza V. Parallel evolution and horizontal gene transfer of the pst operon in Bacillus from oligotrophic environments. Int J Evol Biol. 20112011 doi: 10.4061/2011/781642. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Moreno-Letelier A. Olmedo-Alvarez G. Eguiarte L.E. Souza V. Divergence and phylogeny of Firmicutes from the Cuatro Ciénegas Basin, Mexico: a window to an ancient ocean. Astrobiology. 2012;12:674–684. doi: 10.1089/ast.2011.0685. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Noguez A. Arita H.T. Escalante A.E. Forney L. García-Oliva F. Souza V. Highly structured prokaryotic soil communities in a tropical dry forest. Global Ecology and Biogeography. 2005;14:241–247. [Google Scholar]
  55. Oakley B.B. Carbonero F. van der Gast C.J. Hawkins R.J. Purdy K.J. Evolutionary divergence and biogeography of sympatric niche-differentiated bacterial populations. ISME J. 2010;4:488–497. doi: 10.1038/ismej.2009.146. [DOI] [PubMed] [Google Scholar]
  56. Papineau D. Global biogeochemical changes at both ends of the Proterozoic: insights from phosphorite. Astrobiology. 2010;10:165–181. doi: 10.1089/ast.2009.0360. [DOI] [PubMed] [Google Scholar]
  57. Papke R.T. Ramsing N.B. Bateson M.M. Ward D.M. Geographical isolation in hot spring cyanobacteria. Environ Microbiol. 2003;5:650–659. doi: 10.1046/j.1462-2920.2003.00460.x. [DOI] [PubMed] [Google Scholar]
  58. Peimbert M. Alcaraz L.D. Bonilla-Rosso G. Olmedo-Alvarez G. García-Oliva F. Segovia L. Eguiarte L.E. Souza V. Comparative metagenomics of two microbial mats at Cuatro Ciénegas Basin I: ancient lessons on how to cope with an environment under severe nutrient stress. Astrobiology. 2012;12:648–658. doi: 10.1089/ast.2011.0694. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Pointing S.B. Chan Y.K. Lacap D.C. Lau M.C.Y. Jurgens J.A. Farrell R.L. Highly specialized microbial diversity in hyper-arid polar desert. Proc Natl Acad Sci USA. 2009;106:19964–19969. doi: 10.1073/pnas.0908274106. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Porwal S. Lal S. Cheema S. Kalia V.C. Phylogeny in aid of the present and novel microbial lineages: diversity in Bacillus. PLoS One. 2009;4:e4438. doi: 10.1371/journal.pone.0004438. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Rebollar E.A. Avitia M. Eguiarte L.E. González-González A. Mora L. Bonilla-Rosso G. Souza V. Water-sediment niche differentiation in ancient marine lineages of Exiguobacterium endemic to the Cuatro Cienegas Basin. Environ Microbiol. 2012 doi: 10.1111/j.1462–2920.2012.02784.x. [DOI] [PubMed] [Google Scholar]
  62. Redfield R.J. Do bacteria have sex? Nat Rev Genet. 2001;2:634–639. doi: 10.1038/35084593. [DOI] [PubMed] [Google Scholar]
  63. Roesch L.F.W. Fulthorpe R.R. Riva A. Casella G. Hadwin A.K.M. Kent A.D. Daroub S.H. Camargo F.A. Farmerie W.G. Triplett E.W. Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J. 2007;1:283–290. doi: 10.1038/ismej.2007.53. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Rosenzweig M. Species Diversity in Space and Time. Cambridge University Press; Cambridge: 1995. [Google Scholar]
  65. Seigneur M. Bidnenko V. Ehrlich S.D. Michel B. RuvAB acts at arrested replication forks. Cell. 1998;95:419–430. doi: 10.1016/s0092-8674(00)81772-9. [DOI] [PubMed] [Google Scholar]
  66. Shapiro B.J. Friedman J. Cordero O.X. Preheim S.P. Timberlake S.C. Szabó G. Polz M.F. Alm E.J. Population genomics of early events in the ecological differentiation of bacteria. Science. 2012;336:48–51. doi: 10.1126/science.1218198. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Shurin J.B. Cottenie K. Hillebrand H. Spatial autocorrelation and dispersal limitation in freshwater organisms. Oecologia. 2009;159:151–159. doi: 10.1007/s00442-008-1174-z. [DOI] [PubMed] [Google Scholar]
  68. Silva C. Vinuesa P. Eguiarte L.E. Martinez-Romero E. Souza V. Rhizobium etli and Rhizobium gallicum nodulate common bean (Phaseolus vulgaris) in a traditionally managed milpa plot in Mexico: population genetics and biogeographic implications. Appl Environ Microbiol. 2003;69:884–893. doi: 10.1128/AEM.69.2.884-893.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Silva C. Vinuesa P. Eguiarte L.E. Souza V. Martinez-Romero E. Evolutionary genetics and biogeographic structure of Rhizobium gallicum sensu lato, a widely distributed bacterial symbiont of diverse legumes. Mol Ecol. 2005;14:4033–4050. doi: 10.1111/j.1365-294X.2005.02721.x. [DOI] [PubMed] [Google Scholar]
  70. Sogin M.L. Morrison G.H. Huber J.L. Welch D.M. Huse S.M. Neal P. Arrieta J.M. Hernd G.E. Microbial diversity in the deep sea and the underexplored “rare biosphere.”. Proc Natl Acad Sci USA. 2006;103:12115–12120. doi: 10.1073/pnas.0605127103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Souza V. Eguiarte L.E. Bacteria gone native vs. bacteria gone awry?: Plasmidic transfer and bacterial evolution. Proc Natl Acad Sci USA. 1997;94:5501–5503. doi: 10.1073/pnas.94.11.5501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Souza V. Nguyen T.T. Hudson R.R. Piñero D. Lenski R.E. Hierarchical analysis of linkage disequilibrium in Rhizobium populations: evidence for sex? Proc Natl Acad Sci USA. 1992;89:8389–8393. doi: 10.1073/pnas.89.17.8389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Souza V. Espinosa-Asuar L. Escalante A.E. Eguiarte L.E. Farmer J. Forney L. Lloret L. Rodríguez-Martínez J.M. Soberón X. Dirzo R. Elser J.J. An endangered oasis of aquatic microbial biodiversity in the Chihuahuan Desert. Proc Natl Acad Sci USA. 2006;103:6565–6570. doi: 10.1073/pnas.0601434103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Souza V. Eguiarte L.E. Siefert J. Elser J.J. Opinion—microbial endemism: does phosphorus limitation enhance speciation? Nat Rev Microbiol. 2008;6:559–564. doi: 10.1038/nrmicro1917. [DOI] [PubMed] [Google Scholar]
  75. Stach J.E.M. Maldonado L.A. Masson D.G. Ward A.C. Goodfellow M. Bull A.T. Statistical approaches for estimating actinobacterial diversity in marine sediments. Appl Environ Microbiol. 2003;69:6189–6200. doi: 10.1128/AEM.69.10.6189-6200.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Stackebrandt E. Ebers J. Taxonomic parameters revisited: tarnished gold standards. Microbiol Today. 2006;33:152–155. [Google Scholar]
  77. Tavormina P.L. Ussler W. Joye S.B. Harrison B.K. Orphan V.J. Distributions of putative aerobic methanotrophs in diverse pelagic marine environments. ISME J. 2010;4:700–710. doi: 10.1038/ismej.2009.155. [DOI] [PubMed] [Google Scholar]
  78. Thomas C.M. Nielsen K.N. Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat Rev Microbiol. 2005;3:711–721. doi: 10.1038/nrmicro1234. [DOI] [PubMed] [Google Scholar]
  79. Torsvik V. Ovreas L. Thingstad T.F. Prokaryotic diversity—magnitude, dynamics, and controlling factors. Science. 2002;296:1064–1066. doi: 10.1126/science.1071698. [DOI] [PubMed] [Google Scholar]
  80. Tringe S.G. von Mering C. Kobayashi A. Salamov A.A. Chen K. Chang H.W. Podar M. Short J.M. Mathur E.J. Detter J.C. Bork P. Hugenholtz P. Rubin E.M. Comparative metagenomics of microbial communities. Science. 2005;308:554–557. doi: 10.1126/science.1107851. [DOI] [PubMed] [Google Scholar]
  81. van Passel M.W. Marri P.R. Ochman H. The emergence and fate of horizontally acquired genes in Escherichia coli. PLoS Comput Biol. 2008;4:e1000059. doi: 10.1371/journal.pcbi.1000059. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Venditti C. Meade A. Pagel M. Phylogenies reveal new interpretation of speciation and the Red Queen. Nature. 2010;463:349–352. doi: 10.1038/nature08630. [DOI] [PubMed] [Google Scholar]
  83. Whitaker R.J. Allopatric origins of microbial species. Philos Trans R Soc Lond B Biol Sci. 2006;361:1975–1984. doi: 10.1098/rstb.2006.1927. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Whitaker R.J. Grogan D.W. Taylor J.W. Geographic barriers isolate endemic populations of hyperthermophilic archaea. Science. 2003;301:976–978. doi: 10.1126/science.1086909. [DOI] [PubMed] [Google Scholar]
  85. Wilson C.G. Sherman P.W. Anciently asexual bdelloid rotifers escape lethal fungal parasites by drying up and blowing away. Science. 2010;327:574–576. doi: 10.1126/science.1179252. [DOI] [PubMed] [Google Scholar]
  86. Winsborough B.M. Theriot E. Czarnecki D.B. Diatoms on a continental “island”: Lazarus species, marine disjuncts and other endemic diatoms of the Cuatro Ciénegas basin, Coahuila, México. Nova Hedwigia. 2009;135:257–274. [Google Scholar]

Articles from Astrobiology are provided here courtesy of Mary Ann Liebert, Inc.

RESOURCES