Microbial hitchhikers on intercontinental dust: catching a lift in Chad - PubMed (original) (raw)

doi: 10.1038/ismej.2012.152. Epub 2012 Dec 20.

Ales Lapanje, Adriana Giongo, Suzanne Kennedy, Yin-Yin Aung, Arlette Cattaneo, Austin G Davis-Richardson, Christopher T Brown, Renate Kort, Hans-Jürgen Brumsack, Bernhard Schnetger, Adrian Chappell, Jaap Kroijenga, Andreas Beck, Karin Schwibbert, Ahmed H Mohamed, Timothy Kirchner, Patricia Dorr de Quadros, Eric W Triplett, William J Broughton, Anna A Gorbushina

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Microbial hitchhikers on intercontinental dust: catching a lift in Chad

Jocelyne Favet et al. ISME J. 2013 Apr.

Abstract

Ancient mariners knew that dust whipped up from deserts by strong winds travelled long distances, including over oceans. Satellite remote sensing revealed major dust sources across the Sahara. Indeed, the Bodélé Depression in the Republic of Chad has been called the dustiest place on earth. We analysed desert sand from various locations in Chad and dust that had blown to the Cape Verde Islands. High throughput sequencing techniques combined with classical microbiological methods showed that the samples contained a large variety of microbes well adapted to the harsh desert conditions. The most abundant bacterial groupings in four different phyla included: (a) Firmicutes-Bacillaceae, (b) Actinobacteria-Geodermatophilaceae, Nocardiodaceae and Solirubrobacteraceae, (c) Proteobacteria-Oxalobacteraceae, Rhizobiales and Sphingomonadaceae, and (d) Bacteroidetes-Cytophagaceae. Ascomycota was the overwhelmingly dominant fungal group followed by Basidiomycota and traces of Chytridiomycota, Microsporidia and Glomeromycota. Two freshwater algae (Trebouxiophyceae) were isolated. Most predominant taxa are widely distributed land inhabitants that are common in soil and on the surfaces of plants. Examples include Bradyrhizobium spp. that nodulate and fix nitrogen in Acacia species, the predominant trees of the Sahara as well as Herbaspirillum (Oxalobacteraceae), a group of chemoorganotrophic free-living soil inhabitants that fix nitrogen in association with Gramineae roots. Few pathogenic strains were found, suggesting that African dust is not a large threat to public health.

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Figures

Figure 1

Figure 1

Map of Africa with insets showing the dust/sand collection sites in the Republic of Chad and the Cape Verde Islands. Abbreviations C1—C9 represent the sand collection sites in Chad (see Table 1). WP44, WP45 and WP58 show those in the Bodélé Depression (Table 2) whereas insert (e) shows the positions of the ‘Stad Amsterdam' near the Cape Verde Islands during the storm in which dust was collected (Table 3).

Figure 2

Figure 2

Elemental analyses of desert material collected from the Republic of Chad. (a) Major elements are listed in weight per cent, (b) Trace elements in mg kg−1.

Figure 3

Figure 3

SEM micrographs of air-dried samples of surface material from Chad: Panel (a)=C2; (b)=C1; (c)=C1 magnified; (d)=C3; (e)=C4; (f)=C5; (g)=C6 and (h)=C5. Except for C3, where sand particles were held together by a thick layer of biological material, all other samples were collections of separate sand grains. A great variety of particulate matter can be seen attached to the grains: fragments of diatom shells (arrow) in (c); clumped microbial cells (arrow) in (e); collapsed microbial cells (possibly Archea – arrows in (f); mineral-encrusted microbial filaments (possibly fungal hyphae) in (g) and branched fungal hyphae (arrows) in (h). Different ratios of particulate to biogenic matter and sand grains can be seen in D, where the grains in sample C3 seem to be ‘cemented together' into a surface crust (cf samples C2 (a) and (b) (C1)).

Figure 4

Figure 4

(a) The seven most abundant families of the Phylum Actinobacteria found in the sands of Chad as revealed by HtS (Actinobacterial families making up ⩾0.3% of the total ‘reads' are listed in Supplementary Table 1). Families marked with an asterisk were also found by culture-based methods. Note that the composition of C1 is markedly different from the other samples—more than 50% of the Actinobacteria are Bifidobacteriaceae (anaerobic bacteria of the gastrointestinal tract and vagina), that along with the many Enterobacteriaceae in this sample, undoubtedly came from the large military force garrisoned nearby. (b) HtS based-data showing the seven most dominant families of the Phylum Firmicutes. Families marked with an asterisk were also found by culture-based methods (Supplementary Table 2 lists those families that comprise ⩾0.5% of the total ‘reads'). Again it is obvious that the bacterial composition of C1 differs markedly from the others. Significant numbers of Clostridiaceae (anaerobic to oxygen-tolerant spore-forming bacilli found in soil as well as in normal intestinal flora of animals), Lachnospiraceae (colon inhabitants), Lactobacillaceae (gastrointestinal tract), Streptococcaceae (widely distributed) and Veillonellaceae (gastrointestinal tract) were found. Undoubtedly, their presence is due to human activity nearby. (c) HtS based-data showing the seven most dominant families of the Phylum Proteobacteria. Families marked with an asterisk were also found by culture-based methods (Supplementary Table 3 lists those families that comprise ⩾0.3% of the total ‘reads'). Note that two families that were fairly abundant in samples C2 to C9 were not found in C1. The most prominent of these were the Oxalobacteraceae (that includes the soil/rhizosphere inhabitants Duganella, Herbaspirillum, Naxibacter, Oxalicibacterium and Telluria). Herbaspirillum seropedicae is a well-studied nitrogen-fixing bacterium. Rhodocacteraceae (non-sulphur, purple, photoheterotrophic bacteria) were also noticeably absent. (d) HtS based-data showing the other seven predominant phyla/families apart from those listed in Figure 4 A–C that make up ⩾0.3% of the total ‘reads' in Chad sand (further details are given in Supplementary Table 4). Here again, the bacterial composition of C1 was noticeably different from the rest. Acidobacteria, a widespread and diverse group of mostly soil inhabitants; the Sphingobacteriaceae comprising three genera of environmental bacteria (Mucilaginibacter, Pedobacter and Sphingobacterium) and the Planctomycetaceae, soil and water (both fresh and hyper-saline) bacteria were not detected.

Figure 5

Figure 5

Kingdoms and phyla of Eukaryotes found in samples C3 and C5 by direct HtS methods.

Figure 6

Figure 6

Spearman correlation matrixes between the 40 most abundant bacterial families detected by HtS methods as the principal variable with geographic coordinates and altitude as the supplementary variables. All variables were transformed using log10 to approximate a normal distribution. Red shading represents significant negative correlations; shading in blue signifies positive correlations (α <0.01). Note that the co-occurrence of some bacterial families is strongly positively or negatively correlated at the same location.

Figure 7

Figure 7

Spearman correlation matrix between the 40 most abundant bacterial families detected by HtS methods as the principal variable and geochemical attributes as the supplementary variable. All variables were transformed using log10 to approximate a normal distribution. Red shading represents significant negative correlations; shading in blue signifies positive correlations (α <0.01).

Figure 8

Figure 8

Principal component analyses were performed on the log10 transformed Spearman rank correlation matrices and used to cluster the 40 most abundant bacterial families found by HtS based methods with the geographical coordinates (altitude, latitude and longitude) of the places where samples C1–C9 were collected (see Table 1). Longer vectors indicate a larger contribution of the variable whereas the closer the variables are to one another, the higher the correlation between them.

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