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Microbiota and Host Nutrition across Plant and Animal Kingdoms

2015; Cell Press; Volume: 17; Issue: 5 Linguagem: Inglês

10.1016/j.chom.2015.04.009

1934-6069

Stéphane Hacquard, Rubén Garrido‐Oter, Antonio González, Stijn Spaepen, Gail Ackermann, Sarah L. Lebeis, Alice C. McHardy, Jeffrey L. Dangl, Rob Knight, Ruth E. Ley, Paul Schulze‐Lefert,

Plant-Microbe Interactions and Immunity

Plants and animals each have evolved specialized organs dedicated to nutrient acquisition, and these harbor specific bacterial communities that extend the host's metabolic repertoire. Similar forces driving microbial community establishment in the gut and plant roots include diet/soil-type, host genotype, and immune system as well as microbe-microbe interactions. Here we show that there is no overlap of abundant bacterial taxa between the microbiotas of the mammalian gut and plant roots, whereas taxa overlap does exist between fish gut and plant root communities. A comparison of root and gut microbiota composition in multiple host species belonging to the same evolutionary lineage reveals host phylogenetic signals in both eukaryotic kingdoms. The reasons underlying striking differences in microbiota composition in independently evolved, yet functionally related, organs in plants and animals remain unclear but might include differences in start inoculum and niche-specific factors such as oxygen levels, temperature, pH, and organic carbon availability. Plants and animals each have evolved specialized organs dedicated to nutrient acquisition, and these harbor specific bacterial communities that extend the host's metabolic repertoire. Similar forces driving microbial community establishment in the gut and plant roots include diet/soil-type, host genotype, and immune system as well as microbe-microbe interactions. Here we show that there is no overlap of abundant bacterial taxa between the microbiotas of the mammalian gut and plant roots, whereas taxa overlap does exist between fish gut and plant root communities. A comparison of root and gut microbiota composition in multiple host species belonging to the same evolutionary lineage reveals host phylogenetic signals in both eukaryotic kingdoms. The reasons underlying striking differences in microbiota composition in independently evolved, yet functionally related, organs in plants and animals remain unclear but might include differences in start inoculum and niche-specific factors such as oxygen levels, temperature, pH, and organic carbon availability. The vertebrate gut and plant roots evolved independently in animal and plant kingdoms but serve a similar primary physiological function in nutrient uptake (Figure 1). One major difference between plant and animal nutritional modes is their distinct energy production strategy. Plants are autotrophs, producing their own energy through photosynthesis (carbohydrate photo-assimilates), while animals rely entirely on the energy originally captured by other living organisms (heterotrophs). Long-distance transport mechanisms ensure the distribution of carbohydrate photo-assimilates from chloroplasts in leaves to all other body parts, including roots. Nutrient acquisition by roots to support plant growth is therefore almost exclusively limited to uptake of mineral ions and water from soil. In contrast, the mammalian gut has evolved to facilitate the uptake of simple sugars, amino acids, lipids, and vitamins in addition to ions. It is typically compartmentalized into sections with low microbial biomass in which the products of host enzymatic activity are absorbed (i.e., the human small intestine, SI) and a section for the uptake of microbe-derived fermentation products (human large intestine or hindgut, LI). A significant fraction of the soil nutritive complement and of the dietary intake remains unavailable for plants and animals, respectively, and this defines their dietary constraints. Critical nutrients for plant growth and productivity in soil are nitrogen and phosphorus. However, plant roots can absorb only inorganic nitrogen and orthophosphate (Pi), although phosphorus is abundant in soil both in inorganic and organic pools. Pi can be assimilated via low-Pi-inducible (high-affinity) and constitutive Pi uptake systems (low-affinity) (Lambers et al., 2008Lambers H. Raven J.A. Shaver G.R. Smith S.E. Plant nutrient-acquisition strategies change with soil age.Trends Ecol. Evol. 2008; 23: 95-103Abstract Full Text Full Text PDF PubMed Scopus (313) Google Scholar, López-Arredondo et al., 2014López-Arredondo D.L. Leyva-González M.A. González-Morales S.I. López-Bucio J. Herrera-Estrella L. Phosphate nutrition: improving low-phosphate tolerance in crops.Annu. Rev. Plant Biol. 2014; 65: 95-123Crossref PubMed Scopus (5) Google Scholar). Plant species adapted to neutral or higher soil pH, and more aerobic soils have a preference for nitrate and deploy two nitrate uptake and transport systems that act in coordination. By contrast, plants adapted to low pH (reducing soil) as found in forests or the arctic tundra appear to assimilate ammonium or amino acids (Maathuis, 2009Maathuis F.J.M. Physiological functions of mineral macronutrients.Curr. Opin. Plant Biol. 2009; 12: 250-258Crossref PubMed Scopus (177) Google Scholar). Similarly, a fraction of normal human dietary intake remains undigested and therefore non-bioavailable (fiber). These non-digestible components include plant cell wall constituents such as cellulose, hemicellulose, xylan, and pectin, and certain polysaccharides such as β-glucan, inulin, and oligosaccharides that contain bonds that cannot be cleaved by mammalian hydrolytic enzymes (Tungland and Meyer, 2002Tungland B.C. Meyer D. Nondigestible oligo- and polysaccharides (dietary fiber): their physiology and role in human health and food.Compr. Rev. Food Sci. F. 2002; 1: 90-109Crossref Google Scholar). Plant roots and animal guts are colonized by diverse microbial classes, including bacteria and archaea, fungi, oomycetes, as well as viruses (Table 1). These communities can be regarded as the host's extended genome, providing a huge range of potential functional capacities (Berendsen et al., 2012Berendsen R.L. Pieterse C.M.J. Bakker P.A.H.M. The rhizosphere microbiome and plant health.Trends Plant Sci. 2012; 17: 478-486Abstract Full Text Full Text PDF PubMed Scopus (278) Google Scholar, Gill et al., 2006Gill S.R. Pop M. Deboy R.T. Eckburg P.B. Turnbaugh P.J. Samuel B.S. Gordon J.I. Relman D.A. Fraser-Liggett C.M. Nelson K.E. Metagenomic analysis of the human distal gut microbiome.Science. 2006; 312: 1355-1359Crossref PubMed Scopus (1558) Google Scholar, Qin et al., 2010Qin J. Li R. Raes J. Arumugam M. 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(2013) (metatranscriptomics of rhizosphere samples).PeacTurner et al. (2013) (metatranscriptomics of rhizosphere samples).BarleydBulgarelli et al. (2015) (metagenomics of rhizosphere samples).GuteQin et al. (2010) (metagenomics of gut samples).Bacteria99.3699.459688.577.373.794.0499.1Archaea0.020.02<1<0.5<0.5<0.50.054Eukaryotes0.540.4833.316.620.75.90 2,000 species populate 0.5 g of soil (Schloss and Handelsman, 2006Schloss P.D. Handelsman J. Toward a census of bacteria in soil.PLoS Comput. Biol. 2006; 2: e92Crossref PubMed Scopus (145) Google Scholar). The rhizosphere corresponds to the zone of soil directly influenced by root exudation, while the root compartment can be separated in two distinct niches, rhizoplane and endosphere. The rhizoplane harbors a suite of microbes that tightly adhere to the root surface, while the endosphere is composed of microbes inhabiting the interior of roots. Microbial density is high in the rhizosphere, and species richness gradually decreases along the soil-endosphere continuum (Bulgarelli et al., 2012Bulgarelli D. Rott M. Schlaeppi K. Ver Loren van Themaat E. Ahmadinejad N. Assenza F. Rauf P. Huettel B. Reinhardt R. Schmelzer E. et al.Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota.Nature. 2012; 488: 91-95Crossref PubMed Scopus (233) Google Scholar, Bulgarelli et al., 2015Bulgarelli D. Garrido-Oter R. Münch P.C. Weiman A. Dröge J. Pan Y. McHardy A.C. Schulze-Lefert P. Structure and function of the bacterial root microbiota in wild and domesticated barley.Cell Host Microbe. 2015; 17: 392-403Abstract Full Text Full Text PDF PubMed Scopus (11) Google Scholar, Edwards et al., 2015Edwards J. Johnson C. Santos-Medellín C. Lurie E. Podishetty N.K. Bhatnagar S. Eisen J.A. Sundaresan V. Structure, variation, and assembly of the root-associated microbiomes of rice.Proc. Natl. Acad. Sci. USA. 2015; 112: E911-E920Crossref PubMed Scopus (1) Google Scholar, Lundberg et al., 2012Lundberg D.S. Lebeis S.L. Paredes S.H. Yourstone S. Gehring J. Malfatti S. Tremblay J. Engelbrektson A. Kunin V. del Rio T.G. et al.Defining the core Arabidopsis thaliana root microbiome.Nature. 2012; 488: 86-90Crossref PubMed Scopus (274) Google Scholar) (Figure 1A). Therefore, the bacterial community shifts from a dense and diverse soil-borne community to a host-adapted community with reduced diversity. A spatial heterogeneity of microbial density exists along the digestive track (Stearns et al., 2011Stearns J.C. Lynch M.D.J. Senadheera D.B. Tenenbaum H.C. Goldberg M.B. Cvitkovitch D.G. Croitoru K. Moreno-Hagelsieb G. Neufeld J.D. Bacterial biogeography of the human digestive tract.Sci Rep. 2011; 1: 170Crossref PubMed Scopus (79) Google Scholar). Densities are lowest in the stomach and duodenum (proximal SI) (101–103 bacteria per gram of content) and increase along the length of the SI with a higher density in the distal ileum (104–107 bacteria per gram). Cell densities in the LI can reach 1012–1013 bacteria per gram of content, representing the highest density recorded so far in any environment and exceeding the density detected in the rhizosphere by 2–3 orders of magnitude. Although the density is high, the diversity is relatively low (Stearns et al., 2011Stearns J.C. Lynch M.D.J. Senadheera D.B. Tenenbaum H.C. Goldberg M.B. Cvitkovitch D.G. Croitoru K. Moreno-Hagelsieb G. Neufeld J.D. Bacterial biogeography of the human digestive tract.Sci Rep. 2011; 1: 170Crossref PubMed Scopus (79) Google Scholar, Walter and Ley, 2011Walter J. Ley R. The human gut microbiome: ecology and recent evolutionary changes.Annu. Rev. Microbiol. 2011; 65: 411-429Crossref PubMed Scopus (156) Google Scholar). Using low-error 16S rRNA gene sequencing (LEA-seq) of the human fecal gut microbiota (low depth coverage), the number of bacterial species is estimated at 101 ± 27, which is in alignment with estimates of culture-based techniques (Faith et al., 2013Faith J.J. Guruge J.L. Charbonneau M. Subramanian S. Seedorf H. Goodman A.L. Clemente J.C. Knight R. Heath A.C. Leibel R.L. et al.The long-term stability of the human gut microbiota.Science. 2013; 341: 1237439Crossref PubMed Scopus (223) Google Scholar, Mitsuoka, 1992Mitsuoka T. Intestinal flora and aging.Nutr. Rev. 1992; 50: 438-446Crossref PubMed Google Scholar). Compartmentalization exists also from the inside to the outside of the intestinal tube, defined by the intestinal lumen, mucus, and epithelial surface. Similar to the compartmentalization in the root, a decrease in bacterial density is observed from the lumen to the epithelial surface (Swidsinski et al., 2005Swidsinski A. Weber J. Loening-Baucke V. Hale L.P. Lochs H. Spatial organization and composition of the mucosal flora in patients with inflammatory bowel disease.J. Clin. Microbiol. 2005; 43: 3380-3389Crossref PubMed Scopus (355) Google Scholar, Van den Abbeele et al., 2011Van den Abbeele P. Van de Wiele T. Verstraete W. Possemiers S. The host selects mucosal and luminal associations of coevolved gut microorganisms: a novel concept.FEMS Microbiol. Rev. 2011; 35: 681-704Crossref PubMed Scopus (66) Google Scholar, Zhang et al., 2014Zhang Z. Geng J. Tang X. Fan H. Xu J. Wen X. Ma Z.S. Shi P. Spatial heterogeneity and co-occurrence patterns of human mucosal-associated intestinal microbiota.ISME J. 2014; 8: 881-893Crossref PubMed Google Scholar) (Figure 1B). In the LI, the mucus is subdivided into an inner firmly adherent layer largely devoid of bacteria and an outer layer that is looser and non-adherent and allows some microbial colonization (Johansson et al., 2008Johansson M.E.V. Phillipson M. Petersson J. Velcich A. Holm L. Hansson G.C. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria.Proc. Natl. Acad. Sci. USA. 2008; 105: 15064-15069Crossref PubMed Scopus (482) Google Scholar). A relevant difference for experimentation on the plant root and vertebrate gut microbiota is the ease with which the start inoculum of the root microbiota can be defined. This is due to a predominant horizontal acquisition of root endophytes from the surrounding soil biome, although in some plant species there is evidence for additional vertical transmission of seed-borne endophytes (Barret et al., 2014Barret M. Briand M. Bonneau S. Préveaux A. Valière S. Bouchez O. Hunault G. Simoneau P. Jacques M.-A. Emergence shapes the structure of the seed-microbiota.Appl. Environ. Microbiol. 2014; (Published online December 12, 2014)https://doi.org/10.1128/AEM.03722-14Crossref PubMed Scopus (2) Google Scholar). These endophytes mainly belong to Proteobacteria and can colonize seeds via different colonization routes, including flowers, fruits as well as roots, leaves, and stems (Truyens et al., 2015Truyens S. Weyens N. Cuypers A. Vangronsveld J. Bacterial seed endophytes: genera, vertical transmission and interaction with plants.Environ. Microbiol. Rep. 2015; 7: 40-50Crossref Google Scholar). Even though vertical transmission in mammals is not as explicit as in plants (none are transferred with the germline), vertical transmission nevertheless occurs. The transmission from parent to offspring results from the birth process itself, from milk, and from the close contact that comes from parental care (Unger et al., 2015Unger S. Stintzi A. Shah P. Mack D. O'Connor D.L. Gut microbiota of the very-low-birth-weight infant.Pediatr. Res. 2015; 77: 205-213Crossref PubMed Scopus (6) Google Scholar). In humans, vaginal birth inoculates the newborn with a set of strains that can be matched to the mother, whereas caesarean section results in colonization with skin microbes originating from various caregivers (Dominguez-Bello et al., 2010Dominguez-Bello M.G. Costello E.K. Contreras M. Magris M. Hidalgo G. Fierer N. Knight R. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns.Proc. Natl. Acad. Sci. USA. 2010; 107: 11971-11975Crossref PubMed Scopus (688) Google Scholar). Breast milk is also an important source of microbiota and antibodies that shape the gut microbiome (Newburg and Morelli, 2015Newburg D.S. Morelli L. Human milk and infant intestinal mucosal glycans guide succession of the neonatal intestinal microbiota.Pediatr. Res. 2015; 77: 115-120Crossref PubMed Google Scholar), and introduction of solid foods brings rapid shifts in the bacterial community composition toward an adult-like microbiome (Koenig et al., 2011Koenig J.E. Spor A. Scalfone N. Fricker A.D. Stombaugh J. Knight R. Angenent L.T. Ley R.E. Succession of microbial consortia in the developing infant gut microbiome.Proc. Natl. Acad. Sci. USA. 2011; 108: 4578-4585Crossref PubMed Scopus (377) Google Scholar). Vertical transmission from mother to infant gut microbiota is sometimes behaviorally increased in mammals by feeding mother's fecal matter to their infants. In koalas, for instance, this transmission is believed to participate in the digestion of eucalyptus (Osawa et al., 1993Osawa R. Blanshard W.H. Ocallaghan P.G. Microbiological studies of the intestinal microflora of the koala, Phascolarctos Cinereus 0.2. Pap, a special maternal feces consumed by juvenile koalas.Aust. J. Zool. 1993; 41: 611-620Crossref Google Scholar). Additionally, group living is known to aid the transmission of commensal microbes between members of family groups (humans), troupes (primates), and most likely herds as well. Co-habitation in humans leads to sharing of microbiota, which is enhanced when dogs also co-habit in the same house (Song et al., 2013Song S.J. Lauber C. Costello E.K. Lozupone C.A. Humphrey G. Berg-Lyons D. Caporaso J.G. Knights D. Clemente J.C. Nakielny S. et al.Cohabiting family members share microbiota with one another and with their dogs.eLife. 2013; 2: e00458Crossref Scopus (11) Google Scholar). Ironically, hygiene measures aimed at reducing pathogen transmission may have had broad negative impacts on the transmission of commensals and may underlie the loss of diversity observed in the West (Blaser and Falkow, 2009Blaser M.J. Falkow S. What are the consequences of the disappearing human microbiota?.Nat. Rev. Microbiol. 2009; 7: 887-894Crossref PubMed Scopus (238) Google Scholar). Despite the vast prokaryotic biodiversity found in the biosphere (currently >80 bacterial phyla are described), the host-associated microbiota is dominated numerically by a few phyla. The rhizosphere and the root endophytic compartment of unrelated plant species is often enriched for bacteria belonging to three main phyla (Proteobacteria, Actinobacteria, and Bacteroidetes). In contrast, abundant soil bacteria belonging to the phylum Acidobacteria are excluded from the endophytic compartment (Bulgarelli et al., 2013Bulgarelli D. Schlaeppi K. Spaepen S. Ver Loren van Themaat E. Schulze-Lefert P. Structure and functions of the bacterial microbiota of plants.Annu. Rev. Plant Biol. 2013; 64: 807-838Crossref PubMed Scopus (158) Google Scholar). Compared with the surrounding soil, microbiota members belonging to the phylum Proteobacteria are consistently enriched in the rhizosphere/endosphere compartments of monocotyledonous and dicotyledonous plants, including perennial and annual plants (Bulgarelli et al., 2012Bulgarelli D. Rott M. Schlaeppi K. Ver Loren van Themaat E. Ahmadinejad N. Assenza F. Rauf P. Huettel B. Reinhardt R. Schmelzer E. et al.Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota.Nature. 2012; 488: 91-95Crossref PubMed Scopus (233) Google Scholar, Bulgarelli et al., 2015Bulgarelli D. Garrido-Oter R. Münch P.C. Weiman A. Dröge J. Pan Y. McHardy A.C. Schulze-Lefert P. Structure and function of the bacterial root microbiota in wild and domesticated barley.Cell Host Microbe. 2015; 17: 392-403Abstract Full Text Full Text PDF PubMed Scopus (11) Google Scholar, Edwards et al., 2015Edwards J. Johnson C. Santos-Medellín C. Lurie E. Podishetty N.K. Bhatnagar S. Eisen J.A. 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This likely reflects niche adaptation (nutrient availability, oxygen levels) and the ability to efficiently invade and persist inside or outside the roots of divergent plant species. Firmicutes and Bacteroidetes are by far the two most-abundant phyla detected in adult human and mouse feces. Other phyla represented include the Actinobacteria, Verrucomicrobia, and a number of less-abundant phyla such as the Proteobacteria, Fusobacteria, and Cyanobacteria (Eckburg et al., 2005Eckburg P.B. Bik E.M. Bernstein C.N. Purdom E. Dethlefsen L. Sargent M. Gill S.R. Nelson K.E. Relman D.A. Diversity of the human intestinal microbial flora.Science. 2005; 308: 1635-1638Crossref PubMed Scopus (2625) Google Scholar). Similar to the rhizosphere compartment, the mucus layer of the gut represents a particular niche favoring the proliferation of specialized inhabitants. It has been estimated that at least 1% of the gut microbiota can degrade mucins as a source for carbon and nitrogen (Hoskins and Boulding, 1981Hoskins L.C. Boulding E.T. Mucin degradation in human colon ecosystems. Evidence for the existence and role of bacterial subpopulations producing glycosidases as extracellular enzymes.J. Clin. Invest. 1981; 67: 163-172Crossref PubMed Google Scholar). Select types of bacteria can also attach to mucins, such as Bifidobacterium bifidum, which has the ability to stimulate mucin production via butyrate-induce