Biogeographic responses and niche occupancy of microbial communities following long-term land-use change

doi:10.21203/rs.3.rs-1250532/v1

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Biogeographic responses and niche occupancy of microbial communities following long-term land-use change

https://doi.org/10.21203/rs.3.rs-1250532/v1

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Understanding the effects of forest-to-agriculture conversion on microbial diversity has been a major goal in soil ecological studies. However, linking community assembly to the ruling ecological processes at local and regional scales remains challenging. Here, we evaluated bacterial community assembly patterns and the ecological processes governing niche specialization in a gradient of geography, seasonality, and land-use change, totalizing 324 soil samples, 43 habitat characteristics (abiotic factors), and 16 metabolic and co-occurrence patterns (biotic factors), in the Brazilian Atlantic Rainforest, a subtropical biome recognized as one the world’s largest and most threatened hotspots of biodiversity. We observed no significant shifts in alpha diversity due to land-use change. Meanwhile, pairwise beta diversities and distance decays were lower in pastures than those observed for forest and no-till soils. Pasture communities showed a predominantly neutral model, regarding stochastic processes, with moderate dispersion, leading to biotic homogenization. Most no-till and forest microbial communities followed a niche-based model, with low rates of dispersal and weak homogenizing selection, indicating niche specialization or variable selection. Historical and evolutionary contingencies, as represented by soil type, season, and dispersal process were the main drivers of microbial assembly and processes at the local scale, markedly correlated with the occurrence of endemic microbes. Our results indicate that the patterns of assembly and their governing processes are dependent on the niche occupancy of the taxa evaluated (generalists or specialists). They are also more correlated with historical/evolutionary contingencies and the interactions among taxa (i.e. co-occurrence patterns) than the land-use change itself. Keywords: Biodiversity hotspots, historical contingency, land-use change, microbial distance-decay, microbial niche specialization, soil bacterial co-occurrence.

Biodiversity hotspots

historical contingency

land-use change

microbial distance-decay

microbial niche specialization

soil bacterial co-occurrence

Table 1. Overall topological properties of SparCC networks of co-occurrence between OTUs, following long-term land-use change and seasons.

Network properties	Forest		No-till		Pasture
Network properties	winter	summer	winter	summer	winter	summer
Number of nodes^a	56	34	68	38	113	58
Number of edges^b	87	24	190	24	352	184
Positive edges^c	69	20	158	20	259	125
Negative edges^d	18	4	32	4	93	59
Modularity^e	1.08	1.03	0.78	1.08	1.21	1.17
Number of communities^f	17	16	11	19	18	8
Network diameter^g	6	3	8	3	12	7
Average path length^h	2.67	1.43	2.79	1.41	3.88	2.94
Average degreeⁱ	3.1	1.41	5.58	1.26	6.23	6.34
Av. clustering coefficient^j	0.616	0.45	0.562	0.292	0.569	0.588

^aMicrobial OTUs with at least one significant (P < 0.01) and strong (SparCC > 0.6 or < -0.6) correlation;

^bNumber of connections/correlations obtained by SparCC analysis;

^cSparCC positive correlation (> 0.6 with P < 0.01);

^dSparCC negative correlation (< -0.6 with P < 0.01);

^eThe capability of the nodes to form highly connected communities, that is, a structure with high density of between nodes connections (inferred by Gephi);

^fA community is defined as a group of nodes densely connected internally (Gephi);

^gThe longest distance between nodes in the network, measured in number of edges (Gephi);

^hAverage network distance between all pair of nodes or the average length of all edges in the network (Gephi);

ⁱThe average number of connections per node in the network, that is, the node connectivity (Gephi);

^jHow nodes are embedded in their neighborhood and the degree to which they tend to cluster together (Gephi).

Table 2. Relative contribution of geographic distance, abiotic factors, and biotic factors influencing bacterial communities with different niche occupancies at overall, local, and regional scales. We calculated Pearson product-moment correlations from the simple (Mantel test; 1000 permutations; P < 0.05) and the controlled effects (partial Mantel test; 1000 permutations; P < 0.05). From a set of 64 measured parameters, only non-collinear and significant variables were forward-selected and used in the model. Local and regional microbial communities were selected by the geographic limit for autocorrelation (Moran’s I = 97.196 km; P < 0.05).

Overall communities	Overall scale		Local scale		Regional scale
Overall communities	𝝆	P	𝝆	P	𝝆	P
Geographic distance	0.172	0.001	0.308	0.001	-	-
Abiotic selection	0.135	0.001	0.247	0.001	-	-
Biotic selection	0.292	0.001	0.340	0.001	0.231	0.001
Geographic [Abiotic]	0.131	0.001	0.297	0.001	-	-
Geographic [Biotic]	0.147	0.001	0.260	0.001	-	-
Abiotic [Geographic]	0.073	0.001	0.233	0.001	-	-
Abiotic [Biotic]	0.095	0.001	0.198	0.001	-	-
Biotic [Geographic]	0.278	0.001	0.299	0.001	0.231	0.001
Biotic [Abiotic]	0.277	0.001	0.309	0.001	0.236	0.001
Generalists	Overall scale		Local scale		Regional scale
Generalists	𝝆	P	𝝆	P	𝝆	P
Geographic distance	0.157	0.001	0.285	0.001	-	-
Abiotic selection	0.096	0.001	0.163	0.001	-	-
Biotic selection	0.253	0.001	0.299	0.001	0.206	0.001
Geographic [Abiotic]	0.131	0.001	0.276	0.001	-	-
Geographic [Biotic]	0.134	0.001	0.241	0.001	-	-
Abiotic [Geographic]	0.037	0.003	0.145	0.001	-	-
Abiotic [Biotic]	0.060	0.001	0.114	0.001	-	-
Biotic [Geographic]	0.240	0.001	0.258	0.001	0.206	0.001
Biotic [Abiotic]	0.242	0.001	0.277	0.001	0.210	0.001
Specialists	Overall scale		Local scale		Regional scale
Specialists	𝝆	P	𝝆	P	𝝆	P
Geographic distance	0.160	0.001	0.243	0.001	-	-
Abiotic selection	0.191	0.001	0.325	0.001	-	-
Biotic selection	0.291	0.001	0.356	0.001	0.242	0.001
Geographic [Abiotic]	0.094	0.001	0.229	0.001	-	-
Geographic [Biotic]	0.134	0.001	0.188	0.001	-	-
Abiotic [Geographic]	0.141	0.001	0.315	0.001	-	-
Abiotic [Biotic]	0.155	0.001	0.281	0.001	-	-
Biotic [Geographic]	0.269	0.001	0.324	0.001	0.242	0.001
Biotic [Abiotic]	0.269	0.001	0.318	0.001	0.243	0.001

Table 3. Individual factors influencing bacterial communities with different niche occupancies at overall, local, and regional scales. We calculated Pearson product-moment correlations from the controlled effects ((partial Mantel test; 1000 permutations; P < 0.05). Only non-collinear and significant variables were forward-selected and used in the model. Local and regional microbial communities were selected by the geographic limit for autocorrelation (Moran’s I = 97.196 km; P < 0.05).

Overall communities	Overall scale		Local scale		Regional scale
Overall communities	𝝆	P	𝝆	P	𝝆	P
Spatial distance	0.078	0.001	0.241	0.001	-	-
Elevation	0.030	0.016	0.227	0.001	-	-
Land use	-	-	-	-	0.166	0.001
Soil type	-	-	-	-	-	-
Season	-	-	0.102	0.001	-	-
Biopores	0.085	0.003	0.140	0.001	0.064	0.005
Al3+	-	-	-	-	0.046	0.001
Number of nodes	0.116	0.002	-	-	0.121	0.001
Number of edges	-	-	-	-	0.039	0.043
Negative edges	0.093	0.001	-	-	0.157	0.001
Average weighted degree	0.063	0.007	0.119	0.001	0.046	0.013
Average path length	-	-	0.046	0.002	0.051	0.002
Average clustering coefficient	-	-	-	-	-	-
q-Microbial	-	-	0.063	0.002	-	-
C-Microbial	-	-	0.049	0.010	-	-
Generalists	Overall scale		Local scale		Regional scale
Generalists	𝝆	P	𝝆	P	𝝆	P
Spatial distance	0.058	0.001	0.216	0.001	-	-
Elevation	0.043	0.001	0.228	0.001	-	-
Land use	-	-	-	-	0.131	0.001
Soil type	-	-	-	-	-	-
Season	-	-	0.023	0.005	0.026	0.001
Biopores	0.077	0.006	0.154	0.001	-	-
Al3+	-	-	-	-	0.025	0.013
Number of nodes	0.064	0.019	-	-	0.068	0.004
Number of edges	-	-	-	-	-	-
Negative edges	0.065	0.001	-	-	0.122	0.001
Average weighted degree	0.060	0.016	0.094	0.001	0.052	0.005
Average path length	-	-	-	-	0.048	0.002
Average clustering coefficient	-	-	-	-	-	-
q-Microbial	-	-	-	-	-	-
C-Microbial	-	-	0.038	0.037	-	-
Specialists	Overall scale		Local scale		Regional scale
Specialists	𝝆	P	𝝆	P	𝝆	P
Spatial distance	0.080	0.001	0.201	0.001	0.052	0.001
Elevation	0.019	0.029	0.155	0.001	-	-
Land use	-	-	-	-	0.096	0.001
Soil type	0.032	0.001	0.108	0.001	-	-
Season	0.008	0.028	0.133	0.001	-	-
Biopores	0.036	0.037	0.068	0.001	-	-
Al3+	-	-	-	-	0.072	0.001
Number of nodes	0.205	0.001	0.127	0.001	0.240	0.001
Number of edges	-	-	-	-	0.042	0.006
Negative edges	0.139	0.001	0.039	0.013	0.200	0.001
Average weighted degree	0.041	0.019	0.106	0.001	-	-
Average path length	-	-	0.062	0.001	-	-
Average clustering coefficient	-	-	0.069	0.001	-	-
q-Microbial	-	-	0.063	0.001	-	-
C-Microbial	-	-	-	-	-	-

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First submitted to journal
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Biogeographic responses and niche occupancy of microbial communities following long-term land-use change

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